Invasion of woody species into temperate grasslands: Relationship with abiotic and biotic soil resource heterogeneity

- Invasion of woody species into temperate grasslands - 63Journal of Vegetation Science 18: 63-70, 2007© IAVS; Opulus Press Uppsala.

AbstractQuestion: Invasion of woody species into grasslands is a global phenomenon. This is also topical in semi-natural temp-erate grasslands that are no longer profitable for agricultural management. Trees and grasses interact through harsh root competition, but below-ground processes have been neglected in the dynamics of semi-natural grasslands. Trees are thought to have a competitive advantage in resource-rich and hetero-geneous soils. We tested whether soil resource quantity and heterogeneity differ between paired temperate semi-natural grasslands and forests (former grasslands), and whether this was caused abiotically by varying soil depth or biotically by fine roots.Location: Thin-soil calcareous alvar grasslands with over-grown parts (young Pinus sylvestris forests) in W. Estonia.Methods: The quantity and spatial heterogeneity of soil resources (moisture and nutrients), soil depth, and root para-meters (mass, length and specific length) were measured in 1-m transects of 11 samples in 26 paired grasslands and forests. The quantity and heterogeneity of soil resources were compared between vegetation types and related to soil depth and root parameters.Results: Soil resources were lower and more heterogeneous in forests than in grasslands. The invasion of woody species was enhanced abiotically by deeper soil. Root mass was larger in the forests, but root length was longer in the grasslands. Both root mass and specific root length were more heterogeneous in the forests. Forest root length was negatively correlated with transient soil moisture patches and positively correlated with more persistent nutrient-rich patches. No such relationship was found in grasslands.Conclusions: Abiotic soil heterogeneity (local deep-soil patches) supports woody species invasion, but the trees themselves also biotically make soils more heterogeneous, which further enhances woody species invasion. Large trees use soil resources patchily, making soils biotically poorer and more heterogeneous in resources. The dynamics of temperate semi-natural grasslands are strongly linked to below-ground ecological processes, and high soil heterogeneity can be both the cause and the outcome of woody species invasion.

Keywords: Alvar; Fine root; Grassland conservation; Soil moisture; Soil organic matter; Spatial pattern; Semi-natural ecosystem.

Invasion of woody species into temperate grasslands: Relationship with abiotic and biotic soil resource heterogeneity

Pärtel, Meelis1* & Helm, Aveliina1,2

1Institute of Botany and Ecology, University of Tartu, 40 Lai St., Tartu 51005, Estonia; 2E-mail [email protected]*Corresponding author; Fax +372 7376222; E-mail [email protected]

Introduction

The invasion of woody species into grassland is a global phenomenon (Schlesinger et al. 1990; Van Auken 2000; Roques et al. 2001; Simonson & Johnson 2005). Overgrowing is topical in semi-natural grasslands in the temperate zone, which are characterized by high biodiversity and nature conservation value (Watkinson & Ormerod 2001; Motzkin & Foster 2002; Pärtel et al. 2005a). These ecosystems are presently maintained by the grazing of domestic animals or hay-making, but they consist of a unique set of natural plant species, including many threatened ones (Pärtel et al. 2005b). Semi-natural grasslands are no longer economically profitable, and the cessation of management will lead to the invasion of shrubs and trees (Sutherland 2002; Poschlod et al. 2005). In order to understand the mechanisms of woody species invasion into grasslands, we must compare the ecology of herbaceous and woody life forms (Wilson 1998). Many studies have been performed on the above-ground competition for light, where large woody species have a clear competitive advantage, but the most intense competition takes place below-ground, where the bal-ance between woody and herbaceous vegetation is most likely determined (Wilson 1998; Stevens & Fox 1991). Where above-ground competition depends largely on grassland management (grazing, mowing, burning), below-ground competition depends on soil resource quantity and distribution. Soil resource heterogeneity is linked to several ecological processes (Hutchings et al. 2000). Here we study how soil resource heterogeneity is related to woody species invasion into semi-natural grasslands, and the role of the abiotic and biotic causes of soil heterogeneity. There are several differences between the below-ground structure of herbaceous and woody species. Trees and shrubs have large root systems and they can forage over rich and poor patches. Herbaceous species, in contrast, have small root systems that cannot reach out from poor patches (Campbell et al. 1991; Grime 1994).

64 Pärtel, M. & Helm, A.

Nutrient-rich patches have a limited duration measured in weeks (Farley & Fitter 1999). Thus if a herbaceous species happened to grow in a nutrient-rich patch, this would not guarantee long-term persistence. Conse-quently, the different root distributions of herbaceous and woody species may explain their different affinity to the quantity and heterogeneity of soil resources. The main root characteristics are mass, length and specific length (length divided by mass). Root mass is the most com-monly used root parameter. Fine root length characterizes a plantʼs ability to take up soil resources; specific root length characterizes root architecture (Hodge 2004). The invasion of woody species into grasslands is often related to the increase in soil resource quantity (Wilson 1998). In Poland, for example, soil nitrogen and phosphorus content were higher in young secondary pine woodlands than in adjacent sandy grasslands (Dzwonko & Loster 1997). Similarly, in Canada both soil nitrogen and moisture content were higher in invading Populus tremuloides forest than in neighbouring prairie (Wilson 1993). In African savannas, woody species encroachment leads to an increase in soil nutrient status (Wiegand et al. 2005), but woody species invasion also depends on high rainfall occasions (OʼConnor 1995). The invasion of woody species into temperate grassland has also been explained by increased atmospheric nitrogen pollution (Köchy & Wilson 2001). Thus the difference in resource quantity in forests and grasslands can be caused abioti-cally, e.g. trees preferentially invade richer patches, or biotically by woody species themselves, since plant fine root cycling redistributes nutrients in the soil (Jobbagy & Jackson 2001; Steinaker & Wilson 2005). In addition to soil resource quantity, soil spatial heterogeneity is also related to the dominant vegetation type – in temperate regions, woodlands are more likely to be found on heterogeneous soils, and grasslands on homogeneous soils (Pärtel & Laanisto 2005). High soil resource heterogeneity may support woody species inva-sions (Schlesinger et al. 1990; Kleb & Wilson 1997). Soil resource heterogeneity can be determined abiotically, e.g. due to topography (Kolb & Diekmann 2004) or soil depth (Belcher et al. 1995). Alternatively, woody species can biotically increase soil heterogeneity and thus facilitate their seedlings. For example, woody species can create ʻislands of fertility ̓by foraging a large soil volume but releasing nutrients only under a relatively small canopy (Schlesinger et al. 1996; Pugnaire et al. 2004). In ad-dition, woody species have patchy nutrient uptake and release (Kleb & Wilson 1997; Pärtel & Wilson 2002). Thus, similarly to the quantity of soil resources, soil heterogeneity can also essentially be both abiotic and biotic (Burke et al. 1999). Although the invasion of woody species into semi-natural grasslands has caused much concern, its relation-

ship with soil resource quantity and heterogeneity has not been considered. Grassland species may be much more effective in soil resource acquisition than woody species while the resources are low and homogeneously distributed (Wilson 1998; Pärtel & Wilson 2002). As a model ecosystem we use thin-soil calcareous grasslands (alvar grasslands) that ceased to be managed ca. 30 years ago. In such ecosystems one can easily separate abiotic and biotic influences on soil resource quantity and het-erogeneity. Although these grasslands were not managed for decades, some open grassland patches still remained. The sources of tree seeds are usually nearby, and due to the sparse field layer, alvar grasslands are merely seed-limited and not microsite limited (Zobel et al. 2000). We examine whether the resistance to woody species invasion can be explained by the low and homogeneous soil resources that are unfavourable for trees and shrubs, and whether soil resource quantity and heterogeneity is modified abiotically or biotically. Soil depth over parent rock is the abiotic influence on soil resource quantity and heterogeneity (Belcher et al. 1995). The biotic influence on soil resource quantity and heterogeneity takes place through resource redistribution by fine roots (Jobbagy & Jackson 2001). Using paired sites of well preserved grasslands and former grasslands, now ca. 30-year-old pine forests, we hypothesize that: (1) soil resource (water and nutrients) quantity and heterogeneity are higher in forest than in grassland; (2) forest is located in the abiotically richer and more heterogeneous part of the former grassland; (3) root quantity and heterogeneity are higher in forest than in grassland; (4) soil depth and root length are related to soil resources at the small scale, suggesting a biotic cause of soil heterogeneity.

Material and Methods

We describe the effect of woody species invasion on grassland soil heterogeneity in western Estonia (ca. 58° N, 22-23° E), using alvar grasslands – species-rich calcareous grasslands on shallow soils over Silurian and Ordovician limestone bedrock (Pärtel et al. 1999a; Rosén & van der Maarel 2000). Alvar grasslands have mainly been described in Sweden and Estonia, but similar plant communities are also known from NE North-America (Catling & Brownell 1995) and NW Russia (Znamen-skiy et al. 2006). Overgrowing by woody species is a real concern because the grazing of domestic animals, and cutting shrubs for fuel has decreased significantly during the last century (Pärtel et al. 1999b). In order to determine grassland borders we used historical vegeta-tion maps from the 1930s (Helm et al. 2006). In 26 sites (at least some km between sites) we sampled an open

- Invasion of woody species into temperate grasslands - 65

grassland and adjacent former grassland now overgrown by a 30-year-old pine (Pinus sylvestris) forest. Visually, both open grassland and forest parts had identically flat topography. During the past 30 years grazing pressure has decreased more or less simultaneously in all sites. In recent years grazing has been re-introduced because agri-environment support has become available. We did not include areas where shrub clearing or logging occurred recently. In August 2003 we measured soil depth, moisture, nutrient content and root parameters in central areas of paired grasslands and forests (at least 20 m from the for-est-grassland border). We used 1-m linear transects of 11 samples, with a distance of 10 cm between samples (for all sites 572 samples for both soil and roots). Root and soil measurements to a depth of 3 cm were taken as close as possible to each other (1-2 cm). A scale of 10 cm is comparable with plant rooting patterns in both grasslands and woodlands (Farley & Fitter 1999; Kleb & Wilson 1999). Alvar soils have a homogeneous humus horizon (A, 3-23 cm) above the parent material (C), and the top 3 cm is representative for the whole humus horizon (Pärtel et al. 1999b). Soil depth was measured with a metal stick from the beginning of the mineral soil to the limestone bedrock (1 cm precision). Soil volumetric moisture content was measured using a ThetaProbe (Delta-T Devices Ltd., UK). Due to rain, moisture was measured in 17 grasslands and 18 forests, since uptake by roots cannot be detected in water-saturated soils. Soil samples from the top 10 cm were collected and stored air dry in paper bags until analysed in a soil laboratory. Soil nutrient status was characterized by the organic matter content, which was determined by loss on ignition (organic matter = 0.07 + 0.89 loss on ignition at 360 °C). One sample for soil total nitrogen was taken from all forests and grasslands (Kjeldahl method). Mean organic matter and nitrogen content had a very strong linear relation (r = 0.98, P < 0.001), confirming that soil organic matter content reflects soil nutrient status in general. We determined root parameters from soil cores 3 cm deep and 0.7 cm in diameter (ca. 1 cm2). Samples were stored in plastic bags and frozen until analyzed. Roots were washed in a laboratory and scanned (300 dpi, gray tones) in shallow water in Petri dishes. Im-ages were transformed to black and white and analyzed with the software ʻRootedge ̓(Kaspar & Ewing 1997; Himmelbauer et al. 2004). Root mass, length and specific length were determined for each sample. Root mass was calculated for each sample on the basis of mean root diameter and total root length. For statistics we used mean soil and root parameters from each 1-m transect. For soil depth we used the maximal value within the transect, because widespread

tree roots are often confined to a few deeper soil parts. We used Coefficients of Variation (CV = SD / mean × 100%, Zar 1996) as a measurement of heterogeneity over 11 samples from each grassland and forest. Log10 transformation was used for maximal soil depth in order to obtain normal distribution; no transformations were needed for other variables (Kolmogorov-Smirnov test, P > 0.05). We applied the t-tests for dependent samples to compare same soil and root parameters in paired grasslands and forests. The relationships between abiotic or biotic factors and soil resources are important on a scale that is ̒ recognized ̓by plants, measured in a few cm (Farley & Fitter 1999; Kleb & Wilson 1999). For each grassland and forest we calculated the correlations between soil depth or root length and soil resources (moisture or organic matter content) within the 1 m transect. Due to the low number of replicates (n = 11), we rarely obtained significant results, and due to spatial autocorrelation there may be spurious relationships. We can, however, use our sites as replicates and, with the Sign test, check if there is a tendency for more positive or negative correlations than expected at random.

Results

Moisture content and soil fertility were significantly lower in forests than in grasslands, contrary to initial expectations (Fig. 1). At the same time, soil resources were more heterogeneous in forests than in grasslands. Thus woody vegetation was indeed associated with more heterogeneous soils. Forests had significantly deeper maximal soil depth than grasslands (Fig. 1). At the same time, soil depth heterogeneity did not differ significantly between forests and grasslands. Thus local abiotically richer (deeper) soil patches most likely supported tree invasion. Root mass was twice as large in forests as in grass-lands (Fig. 2). In contrast, both root length and specific root length were much larger in grasslands than in forests. Root mass and specific root length were more hetero-geneous in forests than in grasslands. Variability in root length did not differ between forests and grasslands. Consequently there are striking differences in root pat-terns between temperate semi-natural grasslands before and after woody species invasion. There are more roots in forests regarding biomass, but many more roots regarding length in open grasslands. Forest roots are much more patchily distributed. Compared to random distribution, soil depth was significantly more often negatively related to soil organic matter content, both in grasslands and forests (Table 1). No relationship between soil depth and soil moisture


content was found in grasslands or forests. The root length in forests was more often positively related to soil organic matter content and negatively to soil moisture content than expected at random. In the grasslands no significant relationships were found between root length and soil resource quantity.

Fig. 1. Soil moisture, organic matter content, and soil depth in paired sites of calcareous grassland and forest on former grassland. Quantity (left panels) and heterogeneity within 1 m (CV, Coefficient of Variation, right panels). Open symbols mark statistical means. Results of paired t-tests are indicated, * P < 0.05, ** P < 0.01, ** P < 0.001, N.S. = not significant.


Table 1. Small-scale (1-m transect with 11 samples) relationships between soil depth or root length, and soil resources. The number of positive and negative correlations over different sites are compared using the Sign test. Significant results are indicated in bold.

Relationship Habitat # Pos. # Neg. Z P

Soil depth vs. Soil moisture content Grassland 11 6 1.0 0.332 Forest 12 6 1.2 0.239Soil depth vs. Organic matter content Grassland 6 20 2.5 0.011 Forest 5 21 2.9 0.003Root length vs. Soil moisture content Grassland 12 5 1.5 0.146 Forest 4 14 2.1 0.034Root length vs. Organic matter content Grassland 14 12 0.2 0.845 Forest 22 4 3.3 < 0.001

Fig. 2. Root mass, length and specific root length in paired sites of calcareous grassland and forest on former grassland. Quantity (left panels) and heterogeneity within 1 m (CV, Coefficient of Varia-tion, right panels). Open symbols mark statistical means. Results of paired t-tests are indicated, ** P < 0.01, ** P < 0.001, N.S = not significant.


Discussion

The invasion of woody species into semi-natural grasslands has caused much concern (Pärtel et al. 2005a). Here we showed that grassland overgrowing is related to changes in soil resource quantity and heterogeneity. Contrary to previous expectations, soil moisture and fertility were lower in forests (former grasslands) than in grasslands. In Northern American temperate forest understories, woody species were also more abundant at lower soil resource levels, and herbaceous species at higher soil resource levels (Graves et al. 2006). This can be explained by a higher resource need for herbaceous species that replace their tissues annually. In our forests organic matter has probably been mineralized and soil resources relocated to the relatively large tree canopy (Steinaker & Wilson 2005). In examining soil nutrient dynamics after woody species invasion into grasslands we found a single study from Andean grasslands in which nutrient quantity decreased (Farley et al. 2004). Most studies, however, contradict ours showing higher nutri-ent quantity in forest soils (e.g. Wilson 1993; Dzwonko & Loster 1997; Stark et al. 2003). The relationship be-tween woody species invasion and soil resource quantity may depend on additional factors. For example, studies across precipitation gradients revealed that the invasion of woody species into grasslands increased soil carbon content only at low precipitations, and that soil carbon loss occurred in moist conditions (Jackson et al. 2002). This was linked to a shift in rooting depth and changes in soil biota (nematodes, rhizosphere bacteria and fungi) in low and high moisture conditions. Consequently soil fertility dynamics in relation to tree invasion depends on specific conditions (e.g., moisture, soil depth), and results may even be opposite in different conditions (Guo & Gifford 2002). Resource heterogeneity was much greater in forests than in grasslands (see also Pärtel & Laanisto 2005). Woody species with large root systems have a competi-tive advantage in heterogeneous soils (Campbell et al. 1991; Grime 1994). Our results confirm both abiotic and biotic causes for this relationship. Soil heterogeneity can simultaneously be a cause and an outcome of woody species invasion. Single locations with deeper soil supported the inva-sion of woody species, although soil depth heterogeneity was not significantly related to grassland overgrowth. Since large tree roots can easily reach over the sampled 1 m scale, a single deeper soil location supports the well-being of an individual tree. Trees prefer deeper soils, as shown by studies from Pennsylvanian serpentines (Barton & Wallenstein 1997), Estonian alvars (Pärtel et al. 1999b) and also from Canadian alvars (Schaefer & Larson 1997; Stark et al. 2003). Unlike the present study,

in Canadian alvars soil depth variability was higher in forest than in grassland (Stark et al. 2003). Accordingly, abiotic soil resource variability is important, but not a single determinant of tree invasion. Root parameters differed in grasslands and forests. Root mass was larger in forests, but root length was remarkably higher in grasslands. Specific root length demonstrates striking differences in root morphology in grasslands and in forests: grassland roots are much thinner (Jackson et al. 1997). Spatially, forest roots were more heterogeneously distributed than grassland roots. Evidently trees themselves biotically modify both soil resource quantity and soil heterogeneity. Thus trees have biotically made soil more heterogeneous and favourable for themselves. Soil organic matter was negatively related to soil depth. This may be related to lower microorganism activ-ity in shallow soils, but exact data are lacking. Shallow soils are mostly omitted in studies of soil organic matter (Jobbagy & Jackson 2000). Surprisingly, soil depth was not related to moisture content, showing that the amount of soil moisture is mainly controlled biotically by root activities, and not by abiotic soil volume. In a Canadian alvar study, root competition did not differ across the soil depth gradient, showing also that soil resources are mainly limited biotically by root activity, and not abioti-cally by soil depth (Belcher et al. 1995). The situation may, however, change during the growing season. For example, Canadian prairie soils had higher moisture content than forest soils at the beginning of the grow-ing season, but lower moisture content at the end of the growing season (James et al. 2003). Similarly, shallow soil depth is critical for water availability during very dry periods (Rosén 1995). We found a close relationship between root length and the amount of soil resources, but only in forests. The negative relationship between soil moisture content and root length suggests active water uptake. The positive relationship between soil organic matter content and root length is shown by the concentration of roots in rich patches (Hodge 2004). Controversial results with water and nutrients can be explained by resource patch longevity. Local moisture patches are very transient, and it is most likely that no major root proliferation occurs there. In contrast, plants can recognize more persistent nutrient-rich patches and increase the amount of fine roots there (Pärtel & Wilson 2001). The nutrient-rich patch longevity, however, still lasts for just a few weeks (Farley & Fitter 1999). In summary, the dynamics of temperate semi-natural grasslands are strongly linked to below-ground ecological processes. When acknowledging this aspect, conserva-tion and restoration of desired ecological communities can be more efficient (e.g. see Bakker 2000). In open


semi-natural grasslands, fine grass roots form a dense network and soil moisture and nutrients have very low heterogeneity. In such conditions, herbaceous species can be successful in competition against young woody spe-cies. Abiotic soil heterogeneity (local deep soil patches) supports woody species invasion. After that, large tree canopy is using soil resources patchily, making biotically soils more heterogeneous. High soil resource heterogene-ity will further enhance woody species invasion.

Acknowledgements. We would like to thank the Estonian Science Foundation (grants No. 5503, 6614 and 6619) and the EU 6FP project ALARM (GOCECT-2003-506675) for their support, Tiiu Kupper for her help with the field work, Kristiina Lobjakova for root processing, Tsipe Aavik, Jan Bakker and three anonymous referees for comments.

References

Bakker, J.P. 2000. Environmental heterogeneity: effects on plants in restoration ecology. In: Hutchings, M.J. (ed.) The ecological consequences of environmental heterogeneity, pp. 379-400. Blackwell Science, Oxford, UK.

Barton, A.M. & Wallenstein, M.D. 1997. Effects of Invasion of Pinus virginiana on soil properties in serpentine bar-rens in Southeastern Pennsylvania. J. Torrey Bot. Soc. 124: 297-305.

Belcher, J.W., Keddy, P.A. & Twolan-Strutt, L. 1995. Root and shoot competition intensity along a soil depth gradient. J. Ecol. 83: 673-682.

Burke, I.C., Lauenroth, W.K., Riggle, R., Brannen, P., Madigan, B. & Beard, S. 1999. Spatial variability of soil properties in the shortgrass steppe: The relative importance of topog-raphy, grazing, microsite, and plant species in controlling spatial patterns. Ecosystems 2: 422-438.

Campbell, B.D., Grime, J.P. & Mackey, J.M.L. 1991. A trade-off between scale and precision in resource foraging. Oecologia 87: 532-538.

Catling, P.M. & Brownell, V.R. 1995. A review of the alvars of the great lakes region: distribution, floristic composi-tion, biogeography and protection. Can. Field-Nat. 109: 143-171.

Dzwonko, Z. & Loster, S. 1997. Effects of dominant trees and anthropogenic disturbance on species richness and floristic composition of secondary communities in southern Poland. J. Appl. Ecol. 34: 861-870.

Farley, K.A., Kelly, E.F. & Hofstede, G.M. 2004. Soil organic carbon and water retention after conversion of grasslands to pine plantations in the Ecuadorian Andes. Ecosystems 7: 729-739.

Farley, R.A. & Fitter, A.H. 1999. Temporal and spatial vari-ation in soil resources in a deciduous woodland. J. Ecol. 87: 688-696.

Graves, J.H., Peet, R.K. & White, P.S. 2006. The influence of carbon-nutrient balance on herb and woody plant abundance in temperate forest understories. J. Veg. Sci.

17: 217-226.Grime, J.P. 1994. The role of plasticity in exploiting environ-

mental heterogeneity. In: Caldwell, M.M. (ed.) Exploitation of environmental heterogeneity by plants. Ecophysiological processes above- and belowground, pp. 1-19. Academic Press, San Diego, CA, US.

Guo, L.B. & Gifford, R.M. 2002. Soil carbon stocks and land use change: a meta analysis. Global Change Biol. 8: 345-360.

Helm, A., Hanski, I. & Pärtel, M. 2006. Slow response of plant species richness to habitat loss and fragmentation. Ecol. Lett. 9: 72-77.

Himmelbauer, M.L., Loiskandl, W. & Kastanek, F. 2004. Estimating length, average diameter and surface area of roots using two different Image analyses systems. Plant Soil 260: 111-120.

Hodge, A. 2004. The plastic plant: root responses to heterogene-ous supplies of nutrients. New Phytol. 162: 9-24.

Hutchings, M.J., John, E.A. & Stewart, A.J.A. 2000. The ecological consequences of environmental heterogeneity. Blackwell Science, Oxford, UK.

Jackson, R.B., Mooney, H.A. & Schulze, E.D. 1997. A global budget for fine root biomass, surface area, and nutrient contents. Proc. Natl. Acad. Sci. USA 94: 7362-7366.

Jackson, R.B., Banner, J.L., Jobbágy, E.G., Pockman, W.T. & Wall, D.H. 2002. Ecosystem carbon loss with woody plant invasion of grasslands. Nature 418: 623-626.

James, S.E., Pärtel, M., Wilson, S.D. & Peltzer, D.A. 2003. Temporal heterogeneity of soil moisture in grassland and forest. J. Ecol. 91: 234-239.

Jobbagy, E.G. & Jackson, R. B. 2000. The vertical distribu-tion of soil organic carbon and its relation to climate and vegetation. Ecol. Appl. 10: 423-436.

Jobbagy, E.G. & Jackson, R.B. 2001. The distribution of soil nutrients with depth: Global patterns and the imprint of plants. Biogeochemistry 53: 51-77.

Kaspar, T.C. & Ewing, R.P. 1997. ROOTEDGE: Software for measuring root length from desktop scanner images. Agron. J. 89: 932-940.

Kleb, H.R. & Wilson, S.D. 1997. Vegetation effects on soil resource heterogeneity in prairie and forest. Am. Nat. 150: 283-298.

Kleb, H.R. & Wilson, S.D. 1999. Scale of heterogeneity in prairie and forest. Can. J. Bot. 77: 370-376.

Köchy, M. & Wilson, S.D. 2001. Nitrogen deposition and forest expansion in the northern Great Plains. J. Ecol. 89: 807-817.

Kolb, A. & Diekmann, M. 2004. Effects of environment, habitat configuration and forest continuity on the distribution of forest plant species. J. Veg. Sci. 15: 199-208.

Motzkin, G. & Foster, D.R. 2002. Grasslands, heathlands and shrublands in coastal New England: historical interpreta-tions and approaches to conservation. J. Biogeogr. 29: 1569-1590.

OʼConnor, T.G. 1995. Acacia karroo invasion of grassland - environmental and biotic effects influencing seedling emergence and establishment. Oecologia 103: 214-223.

Pärtel, M. & Laanisto, L. 2005. The effect of herbaceous and woody vegetation on soil nutrient heterogeneity: a global


assessment. In: Erdem, Ü. & Nurlu, R.M. (eds.) X. Euro-pean Ecological Congress Abstracts Book, pp. 109. META Press, Bornova/Izmir, TR.

Pärtel, M. & Wilson, S.D. 2001. Root and leaf production, mortality and longevity in response to soil heterogeneity. Funct. Ecol. 15: 748-753.

Pärtel, M. & Wilson, S.D. 2002. Root dynamics and spatial pattern in prairie and forest. Ecology 83: 1199-1203.

Pärtel, M., Kalamees, R., Zobel, M. & Rosén, E. 1999a. Alvar grasslands in Estonia: variation in species composition and community structure. J. Veg. Sci. 10: 561-570.

Pärtel, M., Mändla, R. & Zobel, M. 1999b. Landscape his-tory of a calcareous (alvar) grassland in Hanila, western Estonia, during the last three hundred years. Landscape Ecol. 14: 187-196.

Pärtel, M., Bruun, H. H. & Sammul, M. 2005a. Biodiversity in temperate European grasslands: origin and conservation. In: Lillak, R., Viiralt, R., Linke, A. & Geherman, V. (eds.) Integrating efficient grassland farming and biodiversity. Grassland Science in Europe 10, pp. 1-14. Estonian Grass-land Society, Tartu, EE.

Pärtel, M., Kalamees, R., Reier, Ü., Tuvi, E.-L., Roosaluste, E., Vellak, A. & Zobel, M. 2005b. Grouping and prioritiza-tion of vascular plant species for conservation: combining natural rarity and management need. Biol. Conserv. 123: 271-278.

Poschlod, P., Bakker, J.P. & Kahmen, S. 2005. Changing land use and its impact on biodiversity. Basic Appl. Ecol. 6: 93-98.

Pugnaire, F.I., Armas, C. & Valladares, F. 2004. Soil as a media-tor in plant-plant interactions in a semi-arid community. J. Veg. Sci. 15: 85-92.

Roques, K.G., OʼConnor, T.G. & Watkinson, A.R. 2001. Dynamics of shrub encroachment in an African savanna: relative influences of fire, herbivory, rainfall and density dependence. J. Appl. Ecol. 38: 268-280.

Rosén, E. 1995. Periodic droughts and long-term dynamics of alvar grassland vegetation on Öland, Sweden. Folia Geobot. Phytotax. 30: 131-140.

Rosén, E. & van der Maarel, E. 2000. Restoration of alvar vegetation on Öland, Sweden. Appl. Veg. Sci. 3: 65-72.

Schaefer, C.A. & Larson, D.W. 1997. Vegetation, environmental characteristics and ideas on the maintenance of alvars on the Bruce Peninsula, Canada. J. Veg. Sci. 8: 797-810.

Schlesinger, W.H., Reynolds, J.F., Cunningham, G.L., Huen-neke, L.F., Jarrell, W.M., Virginia, R.A. & Whitford, W.G. 1990. Biological feedbacks in global desertification. Sci-ence 247: 1043-1048.

Schlesinger, W.H., Raikes, J.A., Hartley, A.E. & Cross, A.F. 1996. On the spatial pattern of soil nutrients in desert ecosystems. Ecology 77: 364-374.

Simonson, J.T. & Johnson, E.A. 2005. Development of the cultural landscape in the forest-grassland transition in southern Alberta controlled by topographic variables. J. Veg. Sci. 16: 523-532.

Stark, K.E., Lundholm, J.T. & Larson, D.W. 2003. Relation-ships between seed banks and spatial heterogeneity of North American alvar vegetation. J. Veg. Sci. 14: 205-212.

Steinaker, D.F. & Wilson, S.D. 2005. Belowground litter con-

tributions to nitrogen cycling at a northern grassland-forest boundary. Ecology 86: 2825-2833.

Stevens, G.C. & Fox, J.F. 1991. The causes of treeline. Annu. Rev. Ecol. Syst. 22: 177-191.

Sutherland, W.J. 2002. Conservation biology: Openness in management. Nature 418: 834-835.

Van Auken, O.W. 2000. Shrub invasions of North American semiarid grasslands. Annu. Rev. Ecol. Syst. 31: 197-215.

Watkinson, A.R. & Ormerod, S.J. 2001. Grasslands, grazing and biodiversity: editors ̓introduction. J. Appl. Ecol. 38: 233-237.

Wiegand, K., Ward, D. & Saltz, D. 2005. Multi-scale patterns and bush encroachment in an arid savanna with a shallow soil layer. J. Veg. Sci. 16: 311-320.

Wilson, S.D. 1993. Belowground competition in forest and prairie. Oikos 68: 146-150.

Wilson, S.D. 1998. Competition between grasses and woody plants. In: Cheplick, G.P. (ed.) Population biology of grasses, pp. 231-254. Cambridge University Press, Cam-bridge, UK.

Zar, J.H. 1996. Biostatistical analysis. Prentice-Hall, London, UK.

Znamenskiy, S., Helm, A. & Pärtel, M. 2006. Threatened alvar grasslands in NW Russia and their relationship to alvars in Estonia. Biodivers. Conserv. 15: 1797-1809.

Zobel, M., Otsus, M., Liira, J., Moora, M. & Möls, T. 2000. Is small-scale richness in a calcareous grassland limited by seed availability or microsite availability? Ecology 81: 3274-3282.

Received 30 March 2006;Accepted 31 August 2006;

Co-ordinating Editor: J.P. Bakker.

Documents

Invasion of woody species into temperate grasslands: Relationship with abiotic and biotic soil resource heterogeneity