Spatial relationships between the standing vegetation

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Spatial relationships between the standing vegetation and the soil seed bank in a fireprone encroached dehesa in Central Spain Iván Torres, Blanca Céspedes, Beatriz Pérez & José M. Moreno

Plant Ecology An International Journal ISSN 1385-0237 Volume 214 Number 2 Plant Ecol (2013) 214:195-206 DOI 10.1007/s11258-012-0159-5

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Author's personal copy Plant Ecol (2013) 214:195–206 DOI 10.1007/s11258-012-0159-5

Spatial relationships between the standing vegetation and the soil seed bank in a fire-prone encroached dehesa in Central Spain Iva´n Torres • Blanca Ce´spedes • Beatriz Pe´rez Jose´ M. Moreno



Received: 17 April 2012 / Accepted: 10 December 2012 / Published online: 20 December 2012  Springer Science+Business Media Dordrecht 2012

Abstract Postfire vegetation regeneration in many fire-prone ecosystems is soil seed bank dependent. Although vegetation and seed bank may be spatially structured, the role of prefire vegetation patterns and fire in determining postfire vegetation patterns is poorly known. Here, we investigated the spatial patterning of species abundance and richness in the vegetation and seed bank of a Mediterranean encroached dehesa in Central Spain. The seed bank was studied with and without a heat shock simulating a spatially homogeneous fire. Semivariograms and cross-semivariograms showed that species richness in the vegetation was aggregated in patches, mainly of herbs, with highest values corresponding to high herb cover and low tree cover. Species richness in the seed bank was also structured in patches, but the spatial pattern was weak. Seedling density of germinates in the seed bank also showed weak spatial pattern. Heating increased overall germination and species richness, and the intensity of the spatial pattern of species richness, particularly of herbaceous species. However, seed bank density patterns disappeared after

Electronic supplementary material The online version of this article (doi:10.1007/s11258-012-0159-5) contains supplementary material, which is available to authorized users. I. Torres (&)  B. Ce´spedes  B. Pe´rez  J. M. Moreno Departamento de Ciencias Ambientales, Universidad de Castilla-La Mancha, Av. Carlos III s/n, 45071 Toledo, Spain e-mail: [email protected]

heat shock because of increased germination of shrubs without spatial pattern. Our results document that the spatial structure of plant richness in the vegetation may persist after fire due to the spatial patterns of herbaceous species in the seed bank, and that postfire species richness patterns can arise independently of fire intensity patterns. However, the spatial structure of the vegetation after fire can be altered by the feedback between shrub encroachment and an eventual fire because of the ubiquitous germination of shrubs. Keywords Land abandonment  Land-use change  Seeder  Semivariogram  Species richness

Introduction Vegetation regeneration after fire commonly proceeds from seeds stored in the soil seed bank, from resprouts or from a combination of the two (Bond and Van Wilgen 1996; Pausas et al. 2004). Soil seed banks are particularly relevant in Mediterranean shrublands, many of which are dominated by seeders, i.e. perennial species whose individuals die during fire, their regeneration depending on seeds stored in the soil (Valbuena and Trabaud 2001). Herbaceous species, most of them annuals, are also a major component of the seed bank in shrublands, and often dominate the postfire flora during the first few years after fire (Kutiel 1997; Pe´rez et al. 2003; Keeley et al. 2005). Yet,

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vegetation dynamics and ecosystem functioning depend not only on species composition and abundance but also on plant spatial patterns (Aguiar and Sala 1999; Ludwig et al. 2005), an issue that until recently has drawn much less attention. Spatial patterns in the vegetation may determine plant–plant interactions, can drive vegetation changes (Miller et al. 2010), or affect fire behaviour through differences in the spatial arrangement of fuel quantity and quality (Duguy et al. 2007), among other. Thus, quantifying spatial patterns in the standing vegetation and in the soil seed bank, and understanding the processes leading to them, is important for better knowing the role of fire on vegetation. Spatial pattern is a common feature of seed banks (Bigwood and Inouye 1988; Henderson et al. 1988; Lavorel et al. 1991; Olano et al. 2002; Caballero et al. 2008) and may be related to the pattern of standing vegetation through its effects on seed rain and seed dispersal (Caballero et al. 2008). Consequently, after fire, patterns in the postfire vegetation may have their origin in the standing vegetation before fire. Despite the above, little is known about how the spatial pattern of species abundance and composition in the soil drives the spatial pattern of the postfire vegetation. Until now, studies have addressed this question by focusing on the spatial aspects of this interaction at the community level in relation to differences in fire intensity (e.g. Segura et al. 1998; Odion and Davis 2000; Stark et al. 2008), while other studies have focused on the spatial pattern at the species level (e.g. Ooi et al. 2006; Perry et al. 2008). It has been suggested that small-scale patterns of fire intensity and subsequent soil heating are determinants of the resulting spatial patterns of seedling emergence after fire (Segura et al. 1998; Odion and Davis 2000). This small-scale patterning of soil heating seems to be strongly related to biomass accumulation in the standing vegetation (Hiers et al. 2009), and the subsequent smouldering combustion of collapsing shrubs during fire (Davis et al. 1989). Therefore, the relationship between fire intensity and postfire spatial patterns in the seed bank mediated by patterns in standing vegetation seems clear, but the importance of the prefire spatial structure of the seed bank remains poorly understood. Understanding the spatial relationships between the standing vegetation and the soil seed bank for plant abundance and species richness in a context of fire is

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particularly relevant for Mediterranean abandoned dehesas. Dehesas are anthropogenic, savanna-like, managed open forests dominated by Quercus species that harbour a great biodiversity and provide important ecosystem services (Maran˜o´n et al. 2009; Bugalho et al. 2011). Dehesas present strong spatial pattern, driven by the presence of trees, which modify the environmental conditions in their surroundings and determine the spatial pattern of herbaceous species, which are the bulk of species (Maran˜o´n et al. 2009; Torres et al. 2012). However, in recent decades, they have been progressively abandoned and have been encroached by shrubs, leading to change in composition and structure of the vegetation, which may disrupt the biophysical gradients created by trees (Brudvig and Asbjornsen 2009) and increase the continuity of fuels and the probability of crown fires (Moreno et al. 1998). Therefore, Mediterranean dehesas are nowadays threatened systems (Bugalho et al. 2011), and it is important to understand the relationships between above- and below-ground plant compartments under the influence of fire. This study examines the spatial structure of species abundance and richness in the standing vegetation and the soil seed bank in an abandoned Quercus suber L. dehesa covered by a seeder-dominated shrubland in Central Spain. The ultimate objective was to learn how the spatial pattern of the vegetation and the seed bank would determine the response to a potential fire in encroached dehesas. We hypothesized that the patterns of species richness would be mainly controlled by herbs, as these are most abundant, and driven by the dominance of the vegetative cover of the main vegetation strata. We expected that species richness in the vegetation would be positively or negatively related to the patterns of herbaceous or woody plant cover, respectively, due to negative interactions between woody plants and herbs. As vegetation patterns commonly influence seed bank patterns, we expected that the seed bank would be dominated by herbaceous plants and that these would exhibit spatial patterns similar to those of the standing vegetation. In order to understand how these patterns would affect postfire regeneration, soil samples were subjected to a heat shock simulating fire. We then hypothesized that the postfire spatial pattern of species richness would decrease in intensity owing to herbaceous species being mostly negatively affected by heat. On the other hand, the pattern of overall seedling abundance would

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increase in intensity owing to elevated germination of seeders after a heat shock, which would be consistent with shrub cover patterns in the standing vegetation.

Materials and methods Study area The study site was located in the vicinity of the village of Anchuras (39270 N, 4520 W, 550 m a.s.l.) in Central Spain. The climate is Mediterranean with a mean annual rainfall of 544 mm, mean minimum temperature of 7.4 C and mean maximum temperature of 20.3 C (Torre de Abraham meteorological station). The vegetation and land use is strongly related to the topographic features: flat areas are cultivated while the slopes of the valleys are covered by cork oak (Quercus suber L.) dehesas that are now abandoned, and are dominated by a dense cover of shrubs, with some open spaces between them still dominated by herbs. The main shrub species are Cistus ladanifer L., Erica arborea L. and Erica australis L., which are accompanied by a rich community of herbaceous plants, mostly annuals. Procedures In July 2006, a 40 9 40 m plot was chosen in a west facing slope (35 % inclination), covered by shrubs and scattered Quercus suber trees, in which no previous fires had taken place for the last decades. Within this plot, 96 1 9 1 m quadrats were laid down, following a randomized nested design. The 40 9 40 m plot was divided into 10 9 10 m quadrats, and within each, six 1 9 1 m quadrats were randomly selected for sampling the standing vegetation and the soil seed bank. The cover of trees, shrubs and herbaceous plants in each quadrat was visually estimated based on the following scale: \1 %, 1–2.5 %, 2.5–5 %, 5–10 %, 10–15 %, 15–20 %, and 10 % increments thereafter. Soil samples which were taken in each 1 9 1 m quadrat (10 soil cores, 3.6 cm diameter, 2.7 cm depth, which were combined to have one sample covering 102 cm2 per quadrat) were brought to the laboratory, air dried at room temperature and passed through a 2-mm sieve to remove rock fragments and other debris. Each sample was divided in two subsamples for subsequent seed bank analysis: one of them (seed

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bank with heat shock, from now on SBH?) was subjected to a heat shock of 100 C during 10 min in a forced-draft oven, after spreading it on a surface of 13 9 20 cm. The heat shock applied is within the range of duration of such temperature in experimental fires in Mediterranean shrublands (Moreno et al. 2011; Ce´spedes et al. 2012). The other subsample was not heated (seed bank without heat shock, from now on SBH-). The size and the composition of the soil seed bank were estimated following the germination method (Thompson et al. 1997). Soil samples were expanded over 13 9 20 cm (260 cm2) plastic trays, with holes in the bottom to evacuate excess water and a layer (ca. 2 cm) of sterilized gardening substrate. This resulted in two soil trays for each quadrat in the field, thus 192 trays. Additionally, control trays (n = 12) containing gardening substrate were set to detect any possible contamination, which was not observed. Trays were kept in a greenhouse to avoid frost and temperatures above 25 C for 10 months, and were watered regularly and rearranged at random every 2 weeks. Germination was checked regularly, plants being removed from the trays as soon as they were identified. After 10 months, soils were dried, crumbled and set over a new layer of substrate to allow germination of any remnant viable seeds until no more germination was recorded 5 months later. Statistical analysis The spatial patterns of plant cover and species richness of the standing vegetation and of number of germinants and species richness of the soil seed bank (unheated and heated) were explored by means of geostatistical analysis. In addition, species richness and seedling abundance data were split into herbaceous and woody species. Data from two quadrats were misplaced, giving a total of 94 quadrats analysed. Geostatistics was selected because it can detect spatial pattern at short distances, and can provide measures of the size and the intensity of the spatial structures. We calculated omnidirectional, experimental semivariograms with a maximum lag distance of 20 m, half the maximum possible distance in the study plot (Rossi et al. 1992). If a trend (i.e. a gradient) was found in the data, detrending was applied by linear regression on the x- or y-coordinates, and the semivariogram of the residuals of the regression was calculated (Legendre and Fortin 1989). Seed bank seedling density and

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species richness data were square-root transformed to attain normality when necessary. In order to facilitate comparisons among the various variables, all experimental semivariograms were modelled with a spherical model (Isaaks and Srivastava 1989). Maximum distance of autocorrelation (range) was calculated from the models, as well as spatial dependence, i.e. the variance in the sample explained by position, which was calculated from the models as the nugget-to-sill ratio (Robertson and Gross 1994). The joint spatial patterns between vegetation cover and species richness or number of germinants were evaluated by means of cross-semivariograms. All calculations were done in R (R Development Core Team 2010). Geostatistical procedures were done with the ‘‘gstat’’ package (Pebesma 2003).

Results The dominant life-form in the standing vegetation was shrubs, which had a mean cover of 56 %. Next were trees, with a mean cover of 27 %. Herbaceous species were scarce in terms of plant cover, with a mean value of 7 % (Table 1). In the seed bank, 1,528 seedlings emerged from the unheated soils and 3,209 from the heated soils, with a mean for woody species of 43 and 71 % in unheated and heated soils, respectively. After the heat shock, Cistus ladanifer accounted for most of the woody seedlings (76 %), while before heating it accounted for only 46 % of all woody seedlings. Erica spp., on the other hand, represented 44 and 21 % of woody seedlings in unheated and heated soils, respectively. This resulted in a mean ± SE of 0.31 ± 0.02 and 0.66 ± 0.03 seedlings cm-2 in SBH- and SBH? soils, respectively (Table 1). We recorded 68 plant species in the standing vegetation, while the total number of species that germinated from the soil samples was 74, both treatments considered. Fiftythree species germinated from unheated soil samples, while 67 species germinated from heated samples. Most of the species found (83 %) were herbaceous (76 % in the vegetation, 89 % in the seed bank), and all the woody species germinating from the seed bank were shrubs. We found a mean species richness in the standing vegetation of 10.8 ± 0.5 species m-2. In the seed bank, we found 6.7 ± 0.3 species tray-1 in SBH- treatment and 7.3 ± 0.3 species tray-1 in SBH? treatment (Table 1). Twenty-one species germinated

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exclusively from the heated soil samples, while 7 species were found germinating from unheated samples solely. Among those species that germinated only in heated samples most were herbaceous generalists, and four of them were Trifolium species. For a complete list of species recorded in the standing vegetation and in the soil seed bank see Torres et al. (2012). Plant cover (trees, shrubs and herbs) in the standing vegetation showed spatial patterning at both long and short distances. Long distance pattern was detected by regression on the x- and y-coordinates (i.e. along and across the main slope, respectively), which was generally very weak (Table 2). An exception was herbaceous cover on the x-coordinate, the direction of maximum slope, which explained 18 % of variance, with greater herbaceous cover in downhill positions. Semivariograms of plant cover (trees, shrubs and herbs) showed strong spatial structure at short distances, with ranges of 11, 9 and 13 m, respectively. Trees were the vegetation layer with strongest spatial structure (89 % of spatial dependence), and shrubs the least intensely structured (49 % spatial dependence), herbs being in between (70 % spatial dependence) (Table 3; Fig. 1). Crosssemivariograms indicated negative spatial relationships between tree cover and herbaceous or shrub cover in the standing vegetation (Table 4). In the seed bank, seedling abundance was spatially structured, mostly at long distances, and linear trends were found along the plot (Table 2). The most noticeable gradient was in relation to the slope, with more seeds appearing in downslope positions. In the case of SBH- a gradient was found across the slope, although this pattern disappeared with the heat shock (Table 2). At short distances, semivariograms showed only a weak spatial pattern of seedling abundance in the unheated samples, which disappeared with the heat shock (Table 3; Fig. 2). However, the patterns of herbaceous and woody seedling abundances differed: herbaceous seedlings showed long distance pattern in both heated and unheated soils, according to regression analysis (Table 2), while woody seedling abundance was not structured at long distances. Herbaceous seedlings were structured in patches of 15–17 m with moderate intensity in heated or unheated soils (Table 3). Woody seedlings, on the other hand, showed spatial pattern at very short distances, which almost completely disappeared (6 % of spatial dependence) with the effect of the heat shock.

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Table 1 Mean (±SE) of herbaceous, woody and total species richness and number of germinants in the standing vegetation, in the soil seed bank without heat shock (SBH-) and in the soil

seed bank after a heat shock simulating a fire (SBH?), based on the 94 1 9 1 m quadrats within the study plot Herbs

Woody

Total

Species richness, standing vegetation

7.09 ± 0.47

3.78 ± 0.13

10.8 ± 0.5

Species richness, SBH-

4.69 ± 0.27

1.99 ± 0.08

6.7 ± 0.3

Species richness, SBH?

4.97 ± 0.27

2.37 ± 0.1

7.3 ± 0.3

Number of germinants (seedlings cm-2), SBH-

0.18 ± 0.02

0.13 ± 0.01

0.31 ± 0.02

Number of germinants (seedlings cm-2), SBH?

0.19 ± 0.02

0.47 ± 0.02

0.66 ± 0.03

Table 2 Regression coefficients (b) and adjusted R2 values of the regressions of plant cover in standing vegetation, species richness in standing vegetation and the seed bank, and number of germinants in the soil seed bank on the x- and y-coordinates of the sampling locations x-Coordinate b

Adj. R

y-Coordinate 2

Adj. R2

b

Standing vegetation cover Herbaceous cover

-0.40

0.18

0.11

0.01

Shrub cover Tree cover

0.59 -0.77

0.05 0.05

0.47 -0.76

0.03 0.04

Number of germinants, total Seed bank, unheated

-0.29

0.16

0.28

0.13

Seed bank, heated

-0.40

0.13

0.02

0.00

Number of germinants, herbaceous Seed bank, unheated

-0.04

0.12

0.02

0.04

Seed bank, heated

-0.04

0.13

0.01

0.00

Number of germinants, woody Seed bank, unheated

-0.01

0.00

0.03

0.11

Seed bank, heated

-0.01

0.02

0.00

-0.01

Total species richness Standing vegetation

-0.17

0.17

0.07

0.02

Seed bank, unheated

-0.08

0.12

0.03

0.01

Seed bank, heated

-0.09

0.14

0.02

0.01

Herbaceous species richness Standing vegetation Seed bank, unheated

-0.15 -0.02

0.16 0.12

0.05 0.01

0.01 0.01

Seed bank, heated

-0.02

0.12

0.00

-0.01

-0.02

0.01

0.02

0.02

0.00

-0.01

0.01

0.00

-0.01

0.00

0.01

0.02

Woody species richness Standing vegetation Seed bank, unheated Seed bank, heated

Significant regressions are italicized

Species richness in the standing vegetation and in the soil seed bank showed spatial structure at several scales. A significant linear trend (i.e. long distance

pattern) was found in species richness in the standing vegetation as well as in the seed bank. This trend was in relation to the slope, and maximum values were found downhill (Table 2). This linear trend, however, was not very strong, and explained 17, 12 and 14 % of variance of species richness in the standing vegetation, SBH- and SBH? soils, respectively (Table 2). In addition, it was exclusively due to herbaceous species richness, while woody species richness showed no gradient (Table 2). At short distances, semivariograms of species richness revealed different degrees of spatial structure in the vegetation and the seed bank. Species richness in the standing vegetation showed strong spatial pattern (63 % spatial dependence) (Table 3; Fig. 3). Both herbaceous and woody species richness presented spatial pattern, but woody species were autocorrelated only at very short distances (ca. 3 m), while the semivariogram of herbaceous species was nearly the same as that of total richness (Fig. 3). In the soil seed bank, species richness was considerably less spatially structured than in the standing vegetation. However, spatial dependence increased with heating, from 9 % spatial dependence in SBH- soils to 25 % in SBH? soils (Table 3; Fig. 3). Maximum autocorrelation distances for species richness increased from near 11 m in the standing vegetation to about 16 m in the seed bank, both in unheated and in heated soils (Table 3). The increase in spatial dependence in total species richness was due to the effect of heat on herbaceous species richness, the spatial dependence of which increased from 8 to 27 % with heat shock. Woody species richness, on the other hand, showed high spatial dependence, but very short distance spatial pattern in both heated and unheated soil samples (Table 3). Based on cross-semivariogram analysis, seedling abundance in the unheated treatment was spatially unrelated, positively related and negatively related to herbaceous, shrub and tree cover, respectively

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Plant Ecol (2013) 214:195–206 and seedling abundance in the soil seed bank without (SBH-) and with (SBH?) a heat shock simulating a fire

Table 3 Model parameters of semivariograms for herbaceous, shrub and tree cover (in the standing vegetation), and for species richness in the standing vegetation and species richness Nugget (C0)

C

Sill (C0 ? C)

Range (m)

C/C0 ? C (%)

R2

Standing vegetation Herb cover

32.5

76.9

109.4

13

70

0.55

Shrub cover

393.6

383.9

777.5

9

49

0.42

Tree cover

156.0

1292.7

1448.7

11

89

0.74

Number of germinants, total Soil seed bank, SBH-

0.6

0.1

0.8

19

19

0.31

Soil seed bank, SBH?













Number of germinants, herbaceous Soil seed bank, SBH-

0.8

0.4

1.1

17

32

0.44

Soil seed bank, SBH?

0.8

0.5

1.3

15

40

0.38

Number of germinants, woody Soil seed bank, SBH0.1

0.6

0.7

4

86

0.32

0.1

1.2

9

6

0.01

Soil seed bank, SBH?

1.1

Total species richness Standing vegetation

7.1

11.8

18.8

11

63

0.67

Soil seed bank, SBH-

0.2

0.0

0.2

16

9

0.16

Soil seed bank, SBH?

0.2

0.1

0.2

15

25

0.22

Herbaceous species richness Standing vegetation

4.4

13.3

17.7

10

75

0.76

Soil seed bank, SBH-

0.2

0.0

0.3

15

8

0.1

Soil seed bank, SBH?

0.2

0.1

0.3

16

27

0.23

Woody species richness Standing vegetation

0.0

1.4

1.4

3

100

0.27

Soil seed bank, SBH-

0.1

0.6

0.7

4

87

0.32

Soil seed bank, SBH?

0.1

0.9

1.0

3

89

0.33

C/C0 ? C is the nugget-to-sill ratio, a measure of spatial dependence (the variance explained by position). All fitted models were spherical – No spherical model could be fit, indicating random spatial pattern

(Table 4; Online resource 1, 2). Herbaceous seedling abundance was positively related to herbaceous and shrub covers, and negatively related to tree cover in both treatments (Table 4). Woody seedling abundance appeared as negatively related to herbaceous cover and positively related to tree cover in both treatments, while it was unrelated and related at very short distances to shrub cover in unheated and heated samples, respectively (Table 4; Online resource 1). Species richness of the standing vegetation was positively related to herbaceous cover, negatively related to tree cover and not related to shrub cover (Table 5). Species richness of the soil seed bank in unheated soils was not related to herbaceous cover, but showed a positive spatial relationship with shrub cover

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and a negative relationship with tree cover. These relationships changed when the soils were heated, so that herbaceous cover was positively related, shrub cover unrelated and tree cover remained negatively related to species richness (Table 5; Online resource 3). Herbaceous species richness, which accounted for most of species, reproduced these patterns: there was a positive relationship with herbaceous cover and richness in vegetation and the seed bank that was weak in the unburned samples but increased with heat shock (Table 5; Online resource 3). The same happened with the negative relationship between tree cover and herbaceous species richness. With shrub cover, a weak positive relationship was found in unheated soils that persisted after heat shock. Woody species richness

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201 Table 4 Sign of the spatial relations, according to crosssemivariograms, between cover of herbaceous plants, shrubs and trees in the standing vegetation, and of number of germinants in the soil seed bank with and without a heat shock simulating a fire Herb cover

Shrub cover

Tree cover

?

-

Vegetation covers Herb cover Shrub cover

?

Total number of germinants Unheated soils



?

-

Heated soils







Herbaceous number of germinants Unheated soils

?

?

-

Heated soils

?

?

-

Woody no. germinants Unheated soils

-



?

Heated soils

-

?

?

For parameters of the fitted models, see Online resource 1 ? positive relation, - negative relation, • no relation

Fig. 1 Experimental semivariograms and models of the cover of herbaceous plants, shrubs and trees in an encroached Mediterranean dehesa

was in most cases unrelated to vegetation cover, and in the rare cases when a model could be fit, goodness of fit was low (Table 5; Online resource 3, 4).

Discussion We found that the standing vegetation drives the spatial patterns of species richness in the seed bank, as

was hypothesized. Biotic interactions between trees and herbaceous plants, in combination with other processes (see later), seem to have been a key in the formation of this spatial pattern. Moreover, our results showed that when a heat shock was applied to the soil, the spatial pattern of species richness persisted, suggesting that spatial patterns may persist after an eventual fire, i.e., postfire spatial patterns in species richness may not be solely dependent on patterns of fire intensity. On the other hand, the spatial pattern of seedling abundance was not as strongly related as the spatial patterns of the standing vegetation. The high germination of woody seedlings, mainly seeders, and the nearly random spatial pattern they exhibited suggest that, in case of fire, shrubs will dominate the whole area irrespective of the factors that shaped their patterns of abundance prior to burning. Because heating was homogeneously applied, such patterns cannot be related to variations in fire intensity. Spatial patterns of seedling abundance or species richness in the soil may be further modified by changes in fire intensity, given the sensitivity of seeds (positive and negative) to changes in this (Moreno and Oechel 1991; Keeley et al. 2008) and to other factors that affect germination in relation to fire products (Izhaki et al. 2000). Nevertheless, our results support that patterns of species richness induced by biotic

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Fig. 2 Experimental semivariograms and models of number of germinations of a all species, b herbaceous species and c woody species in the soil seed bank without a heat shock (left) and subjected to a heat shock (right) of an encroached Mediterranean dehesa

interactions prior to fire may arise, or be enhanced, in postfire environments irrespective of spatial heterogeneity of fire intensity. Spatial analysis showed strong spatial structure of species richness in the standing vegetation, which was mostly due to herbaceous species. Woody species richness, even though it had a strong spatial structure at short distances, contributed little to the overall pattern of species richness. Part of the spatial patterning of species richness was at long distance, following the main topographical gradient of the plot, suggesting an important environmental control on the patterns of species richness (Maltez-Mouro et al. 2005; Legendre et al. 2009). However, the strongest spatial pattern was of small patches, as shown by the model adjusted to the experimental semivariogram. As was expected, the cross-semivariograms showed a positive spatial

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relationship between herbaceous cover and species richness, and a negative one between tree canopies and species richness, thus suggesting greater species richness outside tree canopies, and lower below trees. Analysis by life forms confirmed that these relationships were due exclusively to herbaceous species. These interactions are common in Mediterranean environments, in which trees have been shown to constitute an important source of spatial heterogeneity due to competitive interactions and/or their modification of the microenvironment (Gonza´lez Berna´ldez et al. 1969; Breshears 2006; Shachak et al. 2008). Therefore, the patchy patterns that we found appear to be related to biological interactions between life forms, there being mainly positive feedbacks between herbaceous cover and herbaceous species, and negative ones owing to the competitive exclusion caused

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Fig. 3 Experimental semivariograms and models of a total species richness, b herbaceous species richness and c woody species richness in the standing vegetation and in the soil seed

bank without a heat shock (left) and subjected to a heat shock (right) of an encroached Mediterranean dehesa

by trees on herbs. Shrubs seem to play a minor role in determining spatial pattern of herbaceous species, although the number of herbs may decrease in areas dominated by shrubs (Torres et al. 2012). In the seed bank, a linear trend was also present in the direction of maximum slope, with higher values of species richness downhill than uphill, suggesting a large-scale pattern of seed deposition due to secondary dispersal, probably due to runoff (Ortega et al. 1997). At short distance, and contrary to what could be expected taking into account the strong spatial pattern in the vegetation, the spatial pattern of species richness in unheated soils was weak. This was probably due to the fact that herbaceous species richness showed weak spatial pattern, and most of the species were herbaceous. Woody species richness showed strong spatial pattern at distances of a few meters, but it did not have much influence on the patterns of total richness given

its low values. Notwithstanding, the pattern of herbaceous species richness in the unheated seed bank, although weak, was positively related to herbaceous and shrub cover, and negatively related to tree cover. Thus, our results are partially in agreement with other studies that found spatial structure in the seed bank as a result of the effect of canopy cover (Lo´pez-Pintor et al. 2003; Figueroa et al. 2004; Caballero et al. 2008). Heat shock increased the number of species germinating from the soil samples at the whole plot level. Many Mediterranean species are adapted to fire and are stimulated by exposure to heat, a typical seeder syndrome (Keeley 1991; Pausas et al. 2004). Furthermore, other species without specific fire-related traits have seeds with physical dormancy broken by heat. Indeed, more species emerging from the seed bank after application of heat has been found in a variety of ecosystems (Izhaki et al. 2000; Bossuyt and Honnay

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Table 5 Sign of the spatial relations, according to crosssemivariograms, between cover of herbaceous plants, shrubs and trees in the standing vegetation, and of species richness in the standing vegetation or in the soil seed bank with and without a heat shock simulating a fire Herb cover

Shrub cover

Tree cover

Standing vegetation Unheated soils

? •

• ?

-

Heated soils

?



-

Total species richness

Herbaceous species richness Standing vegetation

?



-

Unheated soils

?

?

-

Heated soils

?

?

-

Woody species richness Standing vegetation





?

Unheated soils

-



?

Heated soils







For parameters of the fitted models, see Online resource 3 ? positive relation, - negative relation, • no relation

2008; Scott et al. 2010). The spatial pattern of species richness in the seed bank not only remained after the heat shock but also enhanced, particularly at short distances. Again, this was due exclusively to the spatial pattern of herbaceous species, which increased from 8 to 27 % spatial dependence, and presented more marked relationships with vegetation cover of the different strata (positive with herbs and shrubs, negative with trees). This suggests aggregation of the herbaceous species that germinated after heat shock. Our results indicate that the spatial pattern of species richness in an unburned stand might be preserved and emerge in the postfire vegetation, particularly those patterns associated with herbaceous species and the cover of herbaceous plants and trees. Therefore, and at least in the short term, the persistence of small-scale spatial pattern in the community is not erased by fire; rather, it seems to be enhanced. In Mediterranean Californian chaparral subjected to experimental burns, Davis et al. (1989) and Odion and Davis (2000) found that the prefire spatial heterogeneity of seed density created by shrub canopies was reinforced by the resulting patterns of soil heating, which were due to differences in biomass accumulation. However, the heterogeneous heating of soils induced by fuel patchiness may be overridden during wildfires under severe fire weather, when flame height and flame depth may

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override the effects of fuel heterogeneity at small scales and produce a homogeneous heating at the soil surface at scales larger than fuel load patterns would suggest (Moreno et al. 2012). Therefore, our simulated homogeneous heating of the soils—the same for all samples regardless of biomass accumulation above them—may well represent natural conditions during high-intensity fires. In this case, pre-existing patterns in the soil seed bank may indeed be very relevant to understand postfire vegetation patterns. In spite of the above, the spatial patterns of seed abundance (i.e. number of seedlings germinated) in the seed bank after the heat shock show a different prospect: The number of seedlings emerging from the heated soils, most of them shrubs (mainly Cistus ladanifer and Erica spp.), germinating in a nearly random spatial pattern, but in high numbers all over the plot, suggest a decoupling of the spatial patterns of shrub cover in the vegetation with the abundance of shrub seeds in the soil. This, however, involves a positive feedback between shrub encroachment and fire. This situation may facilitate further dominance of shrubs, increase fire hazard in the short term and decrease fire return intervals, and put the persistence of trees at stake, facilitating the conversion of dehesa systems into shrublands (Torres et al. 2012; Aca´cio et al. 2009), with the associated long-term modification of the spatial patterns of species richness and of the system itself. Acknowledgments The authors are thankful to J. M. Torrego for permission to work in the field site. A. Velasco provided valuable help at the greenhouse. G. Perry and two anonymous reviewers made valuable comments that helped to improve this manuscript. This project benefitted from funding by the EC FUME project (GA 243888). I. Torres was supported by a FPU grant from the Spanish Ministry of Education and Science (AP 2003-1440).

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