Impact of habitat quality on forest plant species colonization

Forest Ecology and Management 115 (1999) 157±170

Impact of habitat quality on forest plant species colonization Olivier Honnay*, Martin Hermy, Pol Coppin Laboratory for Forest, Nature and Landscape Research, University of Leuven, Belgium, Vital Decosterstraat 102, B-3000 Leuven, Belgium

Abstract The impact of habitat quality and site history on the recolonization potential of ancient-forest plant species on abandoned farmland was studied in the forest of Ename, Flanders, Belgium. With the exception of a network of fringe relics (linear elements mainly along exploitation roads), our study area was cleared and converted to arable land ca. 1850. From 1869 onward, most ®elds were gradually abandoned, resulting in a progressive, partly spontaneous reforestation. Each of the 42 actual forest parcels (amounting to 62 ha) was surveyed and a total of 466 plant species were inventoried. Twenty seven of these were identi®ed as ancient-forest plant species and cataloged in a separate subset. Additionally, the spatial distribution of six ancient-forest plant species (Anemone nemorosa, Corylus avellana, Hyacinthoides non-scripta, Paris quadrifolia, Mercurialis perennis, Vinca minor) was systematically surveyed and digitized in a GIS environment. Habitat quality was assessed on the parcel level using intrinsic soil variables on the one side, and historically related variables (length of the agricultural-occupation period, length of woody fringe relics, and total length of fringe relics s.l.) on the other. Soil texture had a major impact on the duration of agricultural land use after deforestation. Soil phosphate content and pH are positively correlated with the duration of the agricultural land use. The number of ancient-forest plant species was negatively affected by the length of the agricultural-occupation period and soil phosphate content, and positively by the total length of the surrounding fringe relics. The same trends are observed studying the systematically surveyed ancient-forest species. We propose that soil phosphate content affected ancient-forest plant species distribution, because it stimulates vigorous vegetation development and as such has a de®nite effect on evolving competitive plant relationships. Using raster-G.I.S analysis tools, mean and maximum colonization distances and approximate mean and maximum colonization rates per century were calculated for each systematically surveyed species. We conclude that not only seed dispersal capabilities, but also site quality variables play an important role in the colonization process of ancient-forest plant species. In the short term, afforestation of previously heavily fertilized farmland will not result in ¯oristically diverse and, thus, valuable forest habitats. The relatively immobile soil phosphate represents a major barrier. # 1999 Elsevier Science B.V. All rights reserved. Keywords: Historical ecology; Forest ecosystem resilience; GIS; Succession; Ancient-forest plant species

1. Introduction In recent years, the process of herbaceous understory recovery after forest clearcutting has been a point *Corresponding author. Tel.: +32 1632 9749; fax: +32 1632 9760; e-mail: [email protected]

of contention, especially in the United States (Duffy and Meier, 1992; Johnson et al., 1993; Elliot and Loftis, 1993; Bratton, 1994). The disagreements seem to center on the relation between rotation period (length of logging cycle) and recovery potential of the herbaceous understory communities. There remains no doubt that rotation periods, that are too

0378-1127/99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. PII: S0378-1127(98)00396-X

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short to guarantee understory recovery, place an unacceptable mortgage on the future with respect to plant diversity. The situation on the European continent is somewhat different, because the practice of clearcutting ancient-forest has become rather rare (Peterken, 1996). An active afforestation policy is in place, providing a wide range of incentives to establish new forests on lands previously under agricultural occupation. The plant diversity question nevertheless remains: What kind of herbaceous understory communities can we ultimately expect in these new forest communities? The uncertainty exists not only with respect to species occurrence and species richness, but also to species quality. Ancient-forest plant species (sensu Hermy, 1994) are generally con®ned to ancient forests. They are mostly absent in persistent seed banks and have a low colonization potential because of poor seed dispersal capacities and a high sensitivity to disturbance (Rackham, 1980; Peterken and Game, 1984; Hermy, 1992; Wulf, 1994). Because these ancient-forest plants are excellent indicators of the ecological value of forest communities (Peterken, 1974), it is very important to understand the processes underlying their occurrence and abundance, especially on newly forested lands. The objectives of this research can be summarized as follows: 1. The development of an historical ecological approach capable of handling the dif®culties inherent to the study of the spatial dynamics of species with low colonization rates. 2. The assessment of the impact of site history and habitat quality variables on the colonization and establishment rates of ancient-forest plants in a (semi)natural environment. The approach we have taken is based on the assumption that present colonization conditions can be extrapolated from historical disturbance processes and associated forest ecosystem resilience. As such, impact analysis of historical disturbances is directly relevant to the forecasting of deforestation and restoration effects on site-speci®c ecological qualities. The main scienti®c hypothesis therefore can be expressed as follows: Spatial historical dynamics have a major impact on the colonization success rates of ancientforest plant species in recently established forest

communities. Although, the study area selected for this research (forest of Ename, Flanders) is unusual in having a well-documented history (Tack et al., 1993), its ecological characteristics are representative for the lowland forests of Flemish Belgium and other parts of Western Europe. 2. Material and methods 2.1. Study area The forest of Ename occupies 62 ha in the Province of Eastern Flanders, ca. 25 km to the south of Gent (Fig. 1). The annual precipitation is 775 mm and the mean annual temperature 9.58C. The forest itself is located on the eastern side of the river Schelde with altitudes ranging from 14 to 62 m above the sea level. Its northernmost 20% thrives on old, humid alluvial sediments while its southern tip is situated on the silty inter¯uvium between the rivers Schelde and Dender. The bulk of the forest, ca. 75%, occurs on the relatively steep slopes of the ¯oodplain margin on sandysilty soils with a shallow clayey or stony-sandy Tertiary substrate. The dominant tree species are Populus x canadensis Moench, Fraxinus excelsior L., Corylus avellana L., Quercus robur L. and Alnus glutinosa (L.) Gaertn. The forest history of Ename is well documented, back to the year 1063, the year the forest was bought by the abbey of Ename (Tack et al., 1993). However, in the context of this study, we will not go back any further than the period ca. 1851, the years in which major deforestation took place. At that time, the whole forest, with the exception of several linear elements mainly along exploitation roads (fringe relics), was cleared to make place for agriculture. Due to a major crisis in agricultural production in Europe, most ®elds were gradually abandoned from 1869 onwards, resulting in a progressive, partly spontaneous reforestation of the Ename estate. A major part of the forest of Ename was reforested between 1869 and 1887, the leftover after 1916. The last reforestation activity dates from 1969. This particular historical background provides an ideal environment for a (re)colonization study of ancient-forest plant species, many of which survived in the abovementioned fringe relics.

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Fig. 1. Situation of the forest of Ename in Belgium.

2.2. Data collection In all of the 42 parcels that presently make up the forest of Ename, a total of 466 different plant species were inventoried in a 1990 survey. A subset of 27 ancient-forest plant species was identi®ed in agreement with the ®ndings of Rackham (1980), Hermy and Stieperaere (1981), Peterken and Game (1984) and Hermy (1992) and is given in Table 1. Botanical nomenclature is according to De Langhe et al. (1988). At the parcel level, between 0 and 24 of these ancient-forest species were found. For six ancientforest plant species (Anemone nemorosa L., Corylus avellana L., Hyacinthoides non-scripta (L.) Chouard ex Rothm., Paris quadrifolia L., Mercurialis perennis L. and Vinca minor L.), the spatial distribution within the parcels was systematically surveyed using fullcoverage transects (`en tirailleur') and the results were digitized in an Arc/Info geographical information

system (GIS) environment (ESRI, 1995). Fig. 2 illustrates an example of such a data set. It was found that the area occupied at the parcel level by each of these six `indicator' species, did not give evidence of a normal distribution pattern. Log10-transformation of the area (in m2) was necessary. The six species were chosen because they were relatively abundant in the study area and they covered a certain range of dispersal types (Table 1). As a complement to the plant inventory of each of the 42 parcels, soil bulk samples were collected from the upper layer (top 20 cm after litter removal, 5 samples per parcel). Information on 11 soil variables (plant-available Mg, Na, K, Ca and phosphate, Ntot, C (all in mg/100 g soil)), soil pH(H2O) and sand, clay and silt fraction were extracted in the laboratory according to the standard analysis methods of the Belgian Soil Service (Extraction with amoniumlactate and then A.A.S. for the cations, extraction

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Table 1 List of ancient-forest species, occurring in the forest of Ename. Myr: Mymecochore; End: Endo- and Ornitochore; Ane: Anemochore; Hyd: Hydrochore; Epi: Epizoochore; Bar: Barochore Species

Dispersal typea

Acer campestre L. Adoxa moschatellina L. Anemone nemorosa L. Carex remota Jusl. ex L. Carex strigosa Huds. Carex sylvatica Huds. Cornus sanguinea L. Corylus avellana L. Crataegus laevigata L. Dactylorhiza fuchsii (Druce) Soo Dryopteris carthusiana (Vill.) H.P. Fuchs Hyacinthoides non-scripta (L.) Chouard ex Rothm. Lamium galeobdolon (L.) L. Luzula pilosa L. Willd. Lysimachia nemorum L. Melica uniflora Retz. Mercurialis perennis L. Mespilus germanica L. Narcissus pseudonarcissus L. Paris quadrifolia L. Polygonatum multiflorum (L.) All. Primula elatior (L.) Hill Pteridium aquilinum L. Sanicula europaea L. Veronica montana L. Vinca minor L. Viola reichenbachiana Jord. ex Boreau

Ane End Myr Hyd Hyd Myr End End End Ane Ane Bar Myr Myr Ane Myr Myr End Bar End/Myr End Ane Ane Epi Myr Myr Myr

a

Dispersal mode from Ridley (1930), Harper (1977) and Grime et al. (1988).

with amonium-lactate and colorimetric determination for phosphate, Kjeldahl method for N, Walkley and Black method for C.) (Hendrickx et al., 1992). Soil pH and phosphate content were log transformed to meet statistical normality assumptions. In addition, the history of arable land use (length of the agricultural-occupation period) was abstracted from the literature (Tack et al., 1993). Because of the availability of historical maps and documents, it was furthermore possible to distinguish hypothetical three different types of fringe relics (P1, P2, P3), based upon original-site conditions (Tack et al., 1993). A ®rst type (P1) was composed mainly of hedgerow and coppice (probably predominantly Corylus avellana), contrary to a second type (P2) that was characterized by lower shrubs, and a third type (P3) that gave no evidence

of woody components. The ®rst two types together (P1‡ P2) can be referred to as woody fringe relics. All fringe relic positions were digitized into the GIS (Figs. 3 and 4) and total length of fringe relics in a 10 m buffer zone around each of the individual parcels was computed. The buffer zone was necessary to accommodate residual positional inaccuracies in the Arc/Info coverages and their overlay products that could not be corrected for with the available information. Two parcels seemed to be strongly affected by the nearby presence of the outlet of a sewage, and were omitted from the analysis. 2.3. Data analysis All statistical analysis employed the Windows version of SPSS 6.1 (SPSS, 1995). The initial exploratory phase consisted of a factor analysis using a varimax rotation of all the habitat variables. This resulted in four easily interpretable factors, each grouping one set of variables that exhibited a high degree of correlation. Parallel to the factor analysis, a bivariate Pearson correlation analysis was carried out to examine the impact of the length of agricultural-occupation period on the respective soil variables. Next four extracted factors were cross-referenced via partial correlation analysis against the total number of plant species, the number of ancient-forest species, and the spatial distribution of the six indicator species. We then investigated the effects of each individual habitat variable on the same plant distribution variables. All correlation coef®cients were controlled for parcel size. Approximate colonization speeds were then calculated for the six indicator species per parcel. Arc/Info plant distribution and fringe relic maps were rasterized at a 22 m resolution. For each species, distances from each raster cell in which the species occurred to the nearest fringe relic were determined. A new raster layer was generated where cell values represented cell-to-fringe distances. Mean and maximum colonization distances were calculated for each species, ®rst on the basis of all pixel values (forest level) and second at the parcel level. The latter to compute approximate mean and maximum colonization rates by dividing these distances by the number of years since reforestation and by averaging these values for the whole of the forest of Ename. This was done under

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Fig. 2. GIS data layer example on the spatial distribution of Mercurialis perennis, one of the six in detail surveyed indicator ancient-forest species.

Fig. 3. GIS data layer with the spatial distribution and typology of the fringe relics. P1: fringe relic mainly occupied by Corylus avellana; P2: fringe relic occupied by lower shrub; P3: fringe relic with no woody components.

the assumption that colonization started immediately on agricultural abandonment. 3. Results 3.1. Habitat variable analysis Results of the factor analysis of the habitat quality variables are summarized in the ranked rotated factor

matrix represented in Table 2. The matrix comprises four factors with eigenvalues greater than one, allowing us to distinguish four variable groups which can be referred to as `natural mineral condition of the soil' (identi®ed by factor 1), `sandy phase portion in the soil texture' (identi®ed by factor 2), `impact of the duration of agricultural occupation' (identi®ed by factor 3), and `length of fringe relic groups' (identi®ed by factor 4).

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Fig. 4. (a)±(d) Colonization distance frequency distributions and associated curves for four of the indicator ancient-forest species that showed a spatial correlation with the presence of fringe relics.

Table 2 Ranked rotated factor matrix resulting from a PCA of the habitat variables. Four factors were extracted, explaining 74% of the occurring variance Factor 1 Factor 2 Factor 3 Factor 4 Ca Mg Log(pH) Na Ntot Silt Sand K Log (phosphate) Duration Clay P1‡P2 P1‡P2‡P3 Explained variance (%)

0.93 0.85 0.70 0.75 0.68

ÿ0.05 0.23 ÿ0.10 0.07 0.09

0.13 ÿ0.33 0.35 ÿ0.3 ÿ0.34

0.12 ÿ0.11 ÿ0.21 ÿ0.17 0.39

ÿ0.08 ÿ0.20 0.32

ÿ0.93 0.90 0.71

0.22 0.09 ÿ0.13

ÿ0.11 0.06 0.17

0.02 0.10 0.41

0.04 ÿ0.19 0.40

0.85 0.75 ÿ0.51

0.01 ÿ0.30 0.11

ÿ0.06 ÿ0.11 30.1

0.06 0.20 22.2

ÿ0.3 ÿ0.19 12.4

0.87 0.86 9.7

Table 3 gives the correlations between each of the soil properties and the `length of the agricultural occupation period'. Signi®cant positive correlations for soil phosphate, soil silt content and soil acidity and a signi®cant negative correlation for soil clay content were revealed. Silty soils had experienced the longest periods of agricultural occupation, while the opposite was true for most of the clayey parcels. Long-time agricultural land use resulted in increased soil pH and soil phosphate content. Not depicted in Table 3 but also important is that parcels reforested between 1869 and 1887 had lower phosphate concentrations (average 4.10 mg/100 g soil) and presented no gradual increase in soil phosphate, those that were reforested between 1916 and 1969 did show evidence of increased phosphate gradients (average: 10.11 mg/ 100 g soil, Mann±Whitney p-value for difference in mean ranks between the two groups of parcels: p<0.001).

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Table 3 Bivariate correlations between the length of the agricultural-occupation period and soil properties of a parcel (nˆ40) Soil properties

Clay fraction

Silt fraction

Sand fraction

Ca

Log(pH)

K

Mg

Na

Log (phosphate)

Ntot

Length of the occupation period

ÿ0.39a

0.37a

ÿ0.15

0.13

0.36a

ÿ0.28

ÿ0.24

0.20

0.71b

ÿ0.30

a b

0.01ˆ
Table 4 Partial correlations between the factor scores of each parcel (see Table 2) and the total number of ancient-forest species and the log(area) of the indicator ancient-forest species. The data sample for Paris quadrifolia was not large enough and allowed no statistical analysis. The correlation with the total number of species is given as a referencea

Total number of species Number of ancient-forest species Log(Vinca) (neˆ16) Log(Anemone) (nˆ37) Log(Corylus) (nˆ27) Log(Hyacynthoides) (nˆ29) Log(Mercurialis) (nˆ15)

Factor scores on factor 1

Factor scores on factor 2

Factor scores on factor 3

Factor scores on factor 4b

0.42c 0.15 0.67c ÿ0.09 0.07 ÿ0.41d 0.02

ÿ0.36d 0.17 0.07 0.05 ÿ0.08 0.04 ÿ0.56d

0.04 ÿ0.46c 0.16 ÿ0.62f ÿ0.56c ÿ0.05 0.01

0.08 0.26d 0.20 ÿ0.06 ÿ0.06 0.33d 0.69c

a

The correlations are controlled for the area of the parcel. One tailed significance. c 0.001ˆ
3.2. Plant species pattern and habitat quality variables Initially, we were interested in the impact on ancient-forest species distribution of the natural soil properties (factors 1 and 2) and the historical parameters (factors 3 and 4). Factor scores for each of the 40 parcels were calculated and related to the total number of species (primarily for reference purposes), total number of ancient-forest species, and log(area) of the six indicator species (Table 4). The correlation between the total number of species and factors 1 and 2 was signi®cant. The same applied to the number of ancient-forest species and factors 3 and 4. With respect to plant cover, factor 1 in¯uenced the abundance of Vinca minor and Hyacinthoides non-scripta. Factor 2 did the same with Mercurialis perennis. Factor 3 signi®cantly affected the occurrence of Ane-

mone nemorosa and Corylus avellana, and factor 4 evidently had a direct bearing on the distribution of Hyacinthoides non-scripta and Mercurialis perennis. Table 5 lists the correlations between the individual habitat variables and species distribution. The relationship between total length of fringe relics (P1‡P2‡P3) and number of ancient-forest species was signi®cantly positive, contrary to the duration of agricultural occupation and soil phosphate content which seem to have an opposite (signi®cantly negative) effect. No correlations between the number of ancient-forest species and any of the other habitat quality variables were signi®cant at the 0.05 level. An analogous analysis for the total number of plant species indicated a similarly signi®cant positive correlation with soil calcium content and with soil pH. No signi®cant correlation was found with the total length of fringe relics and the length of the occupation period.

164

Number of plant species Number of ancient woodland species LOG(Anemone) (ngˆ37) LOG(Mercurialis) (nˆ15) LOG(Vinca) (nˆ16) LOG(Corylus) (nˆ27) LOG(Hyacinth.) (nˆ29) a

P1‡P2b

P1‡P2‡P3b

Duration occupation

Log (phosphate)

Log(pH)

Clay

Silt

Sand

ÿ0.05 0.24d

ÿ0.09 0.46f

0.02 ÿ0.47c

ÿ0.01 ÿ0.46c

0.46c ÿ0.11

ÿ0.02 0.26d

0.29d ÿ0.27d

ÿ0.37e 0.15

0.49f 0.11

ÿ0.12 0.68c 0.60c 0.04 0.10

0.23d 0.68c ÿ0.26 0.30d 0.47c

ÿ0.70c ÿ0.23 0.11 ÿ0.50c ÿ0.46c

ÿ0.36c ÿ0.18 ÿ0.09 ÿ0.55c 0.20

ÿ0.31d ÿ0.01 0.44d ÿ0.31 ÿ0.51c

ÿ0.02 ÿ0.04 0.50d 0.17 ÿ0.38e

ÿ0.06 0.43 ÿ0.24 0.00 0.06

0.09 ÿ0.56e ÿ0.14 ÿ0.11 0.23

ÿ0.20 0.23 0.70c ÿ0.04 ÿ0.48c

The correlations are controlled for the area of the parcel. One tailed significance test. c 0.001ˆ
Ca

K ÿ0.15 0.28d 0.14 ÿ0.21 0.32 0.15 ÿ0.08

Mg 0.31e 0.29d 0.12 ÿ0.17 0.54e 0.20 ÿ0.38e

Na 0.06 0.23 ÿ0.04 ÿ0.12 0.65c 0.08 ÿ0.33d

Ntot 0.20 0.25 0.11 ÿ0.21 0.24 0.14 0.05

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Table 5 Partial correlations between the environmental variables and the total number of ancient-forest species and the log(area) of the five indicator ancient-forest species. The data sample for Paris quadrifolia was not large enough and allowed no statistical analysis. The correlation with the total number of species is given as a referencea

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Total length of fringe relics (P1‡P2‡P3) and/or total length of woody fringe relics (P1‡P2) was signi®cantly correlated to the spatial distribution of three out of the six indicator plant species: Mercurialis perennis, Vinca minor and Hyacinthoides non-scripta. The data sample for Paris quadrifolia was too small to allow for any statistical analysis. Visual assessment indicates a positive correlation between the plant species and the length of the woody fringe relics. Anemone nemorosa and Corylus avellana have signi®cant negative correlations with soil phosphate and length of the agricultural occupation period, while not showing any evidence of a signi®cant link to woody fringe relic length or simply fringe relic length at the 0.05 level (a slight correlation (p<0.1) with total fringe relic length seems to exist, however). The length of the occupation period also in¯uences Hyacinthoides non-scripta. Table 5 suggests that the other soil variables play only a minor role in the spatial distribution of the indicator species. 3.3. Colonization distances from fringe relics and colonization rates Average and maximum colonization distances to the nearest fringe relic sensu lato, and average and maximum colonization rates per century were calculated for only four out of the six indicator species, (Table 6) i.e. those which exhibited a clear spatial relation with the fringe relics. Colonization distance frequency distributions and associated curves showed a typically monotonic curve for Mercurialis perennis and Hyacinthoides non-scripta but unimodal patterns for Paris quadrifolia and Vinca minor.

165

4. Discussion The factor analysis indicates that the habitat quality variables that affect the distribution of ancient-forest plant species can be grouped into: those associated with natural soil condition (factors 1 and 2) and those connected to site history (factors 3 and 4). This is not an unexpected conclusion (Brunet, 1993). However, there are other relationships that may be inferred from the data analysis and that are of particular interest with respect to the colonization and dispersal potential of forest plant species in newly-established forests. 4.1. Soil properties of forest parcels and prior land use The relationship between soil texture and length of the agricultural-occupation period clearly illustrates that arable land use occupation patterns were ultimately governed by physical soil properties. While the most clayey parts of the estate of Ename, situated on alluvial Schelde or on barren tertiary substrates, were the ®rst to be abandoned by agricultural practice, the opposite is true for the sites covered by a thick eolic silt layer. The relationship with soil phosphate content and soil pH re¯ects, the long-term effect of agricultural land use (and fertilization) on soil conditions after reforestation. Parcels that remained the longest under arable land use (reforested after 1916) still exhibit increased soil phosphate content and soil pH in contrast to those reforested between 1869 and 1887. With respect to other land uses, literature sources reveal, however, that (total) soil phosphate content returned to normal 5±13 years after reconversion of arable land to, for example, heathland (Pywell et al.,

Table 6 Average and maximal colonization distances and rates from the nearest fringe relic for four out of the six indicator ancient-forest speciesa Ancient-forest plant species

Maximal distance dmax (m)

Average distance dav (m)

Max. col. rate 1/n dmax i/ti (m/century)

Av. col. rate 1/n dav i/ti (m/century)

Mercurialis perennis Hyacinthoides non-scripta Paris quadrifolia Vinca minor

84 84 74 50

14 23 25 13

28 55 32 30

22 32 21 16

a

dmax: Maximal colonization distance on the forest level; dav: Average colonization distance on the forest level; dmax i: Maximal colonization distance in parcel i; dav: Average colonization distance in parcel i; ti: Time since reforestation of parcel i; n: Number of parcels where the species occurs.

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1994), or that ca. 12 years were necessary to normalize soil phosphate content of abandoned farmland to that of semi-natural grassland condition (Gough and Mars, 1990). Although soil phosphate-analysis methods differ between these and our studies, this may suggests that the conversion of agricultural land to forest cover has a more prolonged impact on soil phosphate concentration than other land use destinations. Consequently, one may say that soil phosphate mapping can provide a good assessment of former land use and associated farming activity and can, therefore, be considered an ecologically meaningful indicator, as is also suggested by archaeological research (Gebhardt, 1982). On the other hand, prior agricultural land use left no traces of increased soil nitrogen content in any of the parcels studied. A possible and probable explanation is the high mobility (due to leaching and volatilization) of this compound (Aulakh et al., 1992). 4.2. Ancient-forest plant species diversity and site history Just as Peterken and Game (1984) concluded from their investigation in Central Lincolnshire (UK), our research reveals that distribution of some plant species is affected by land use history. More speci®cally, the distribution pattern of ancient-forest plants is clearly linked to the occurrence of fringe relics. From these refuges, recolonization of abandoned farmland by forest species was possible. That the correlation between occurrence of fringe relics and the presence of ancient-forest species is still strong after 100 years of recolonization proves, however, the poor recolonization potential of these species. As is further discussed, this may be explained by restricted plant dispersal characteristics and/or disturbance-sensitivity factors (Peterken and Game, 1984; Hermy, 1994). Also, the lack of a persistent seed bank may hamper the re-establishment of certain forest plant species (Warr et al., 1994). In the eastern USA, Matlack (1994) found that plant migration rates are directly affected by dispersal mechanisms. He proposed the following ranking of these mechanisms in the order of diminishing success: dispersal by seed ingestion; dispersal by seed adhesion; wind dispersal; dispersal by ants; and no speci®c dispersal mechanism. Only seven of the ancient-forest species are dispersed via ingestion or adhesion by mammals or birds (Table 1). The majority is dispersed

by ants or gravity (12 species); six are dispersed by wind, hardly an effective mechanism in a forest environment. Ancient-forest species seed banks are not persistent either. This comes as no surprise, since they form part of a climax vegetation type (Warr et al., 1994). It follows that disturbance may have dramatic effects on the survival of ancient-forest species, which is the reason they are referred to as extinction-prone (Peterken, 1974). The notion that forest species survive in `ghost hedges' after deforestation is not new (Pollard, 1973; Forman and Baudry, 1984). With respect to the six indicator species of this study, this phenomenon has been cited for Mercurialis perennis (Pigott, 1977; Rackham, 1980; Peterken and Game, 1981), Hyacinthoides non-scripta (Pigott, 1977; Rackham, 1980) and for Anemone nemorosa (Rackham, 1980; Peterken, 1981). Rackham (1980) argues that as forest is converted into grassland, forest species, including ancient-forest species, such as Mercurialis perennis, persist in meadows, but not in pasture and arable land. He suggests that ``many plants of ancient-forests do not require shade in the ®rst place, but freedom from grazing, plowing, the competition of tall herbs and the axe''. For most of the ancient-forest species on the Ename estate, the mere presence of relic fringes seems to have guaranteed species survival, even after several decades of surrounding agricultural land use. Soil phosphate is also a determining factor in the recolonization process of ancient-forest species. Our analyses show a negative correlation between average soil phosphate content of the forest parcel and the total number of ancient-forest species inventoried per parcel (species diversity). Phosphate contents of 10 mg per 100 g of soil or more, seem to curtail species diversity signi®cantly. While, Wulf (1994) observed a mean phosphate content of only 2 mg per 100 g of soil in 127 ancient woodland soils in Germany, this parameter averages 5 mg per 10 g of soil in Ename, with a range of 2±23 mg and a standard deviation of 3.5 mg. It is, however, unlikely that soil phosphate content itself is the sole factor inhibiting recolonization by ancient-forest species. Various sources (e.g. Peterken, 1981; Grime et al., 1988) have con®rmed that secondary effects, such as vigorous ground vegetation development, against which ancient-forest species are unable to compete, represent a forbidding barrier. Pigott (1971) wrote that phosphate rather than nitrate

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stimulated the establishment of the common and dominant species Urtica dioca L., thus rendering the chances for recolonization by ancient-forest species very slim. In an inventory of 640 forest parcels in 180 different forests in western Belgium, Hermy et al. (1993) substantiated this claim by proving the negative correlation between Urtica dioca cover and ancient-forest species diversity. Kubikova (1994) attempted to enrich the species diversity in secondary forests by transplanting small top-soil segments from ancient forests together with their established vegetation, e.g. Mercurialis perennis, Hepatica nobilis Schreb and Lathyrus vernus (L.) Bernh. She noticed that 7 years later, most transplanted species had survived but had not transgressed the segment boundaries. While unfortunately, phosphate content differences were not analyzed in this study, soil pH and nitrate content differences between segment and surrounding secondary forest soil remained even after 7 years. In addition, colonization of the implanted soil segment by ruderals, such as Impatiens parvi¯ora DC. was observed. The same author also concluded that ancient-forest plant species are victims of the competitive exclusion by ruderal posphateophiles, such as Lapsana communis L. and Alliaria petiolata (Bieb.) Cavara et Grande. Our research indicates that at the parcel level, ancient-forest species diversity is negatively affected by the length of the agricultural-occupation period. We suggest that the in¯uence of the latter variable is indirect and it is primarily the soil phosphate content that increases, that is correlated with the duration of arable land use, and causes the phenomenon. However, there may also be other factors that play a role and that are not directly re¯ected in one or more of the measured top-soil properties. Froment and Tanghe (1967) reported a negative impact of soil disturbance during agricultural occupation (e.g. compaction of the upper-soil layer and ensuing change in hydrological soil regime) on the recolonization of Narcissus pseudonarcissus L., Mercurialis perennis, and Orchis mascula (L) L. in the Belgian Ardennes. 4.3. Ancient-forest plant species diversity and natural soil conditions The relationship between ancient-forest plant species diversity and local soil conditions is much weaker

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than that between diversity and historical variables (Table 5). From the available data, one may conclude that soil condition factors are of minor relevance with respect to ancient-forest plant diversity and have a little value as distribution predictors. 4.4. Indicator species distribution patterns The fact, that the occurrence of four out of the six indicator plants, Mercurialis perennis, Vinca minor, Paris quadrifolia and Hyacinthoides non-scripta, is still correlated with the presence of either or both of the fringe types, woody fringe relics (P1‡ P2) and fringe relics sensu lato (P1‡ P2‡ P3), testi®es to the rather slow colonization rate of the four species. The distribution pattern of Hyacinthoides non-scripta and Mercurialis perennis is associated with the presence on the parcel boundaries of fringe relics sensu lato. For Vinca minor and Paris quadrifolia, non-woody fringe relics appear to have been insuf®cient to safeguard their survival during the periods of agricultural occupation of the parcel. As to the reason behind, these slow colonization rates, Vinca minor and Mercurialis perennis (according to Peterken and Game (1981), also a vegetative spreader) are myrmecochores which limits their dispersal ranges. Ridley (1930) identi®ed Paris quadrifolia as a diplochore with both, ants and birds as dispersal agents. The analysis of our data shows restricted colonization distances and does not exhibit any evidence of dispersal by birds. Hyacinthoides non-scripta is commonly classi®ed as a barochore and this is con®rmed by our results. The distribution patterns of the two other indicator plants, Anemone nemorosa and Corylus avellana, show little evidence of fringe relic impact, but are clearly affected by soil phosphate content and the length of the agricultural-occupation period. Anemone nemorosa is a vegetative colonizer (Grime et al., 1988) and also, a myrmecochore. The species, moreover, lacks a persistent seed bank. However, the lack of any residual correlation with fringe relic presence in the forest of Ename, points to either a relatively fast recolonization speed or another dispersal/survival mechanism. The ®rst hypothesis has been con®rmed in other sites by various researchers. Froment and Tanghe (1967) observed Anemone nemorosa as the ®rst geophyte to colonize abandoned farmland. Falinski and Canullo (1985) also noticed its high

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colonization rate (600 m in 20 years) on land, previously under agricultural occupation in Bialowieza Forest. The premise of these authors is that, zoochory (deer and wild boar) played a major role in seed dispersal. Small mammals may have played a similar role in the forest of Ename. The second hypothesis suggests that Anemone nemorosa was able to weather the agricultural occupation on the land itself. This geophyte with its super®cial rhizomes survived the extensive agricultural land use of the 19th century in situ and was able to recolonize the parcel from within on abandonment. A similar phenomenon, namely the survival of geophytes in land under agricultural occupation, had already been noticed by the Flemish botanist Dodoens (1618). Because Corylus avellana seeds (nuts) are easily dispersed by small mammals (Kollmann and Schill, 1996) correlation with the occurrence of any form of fringe relics in the forest of Ename is very weak. There is, however, a signi®cant negative impact of soil phosphate content on the distribution pattern of the two species. During their Anemone nemorosa colonization research, Falinski and Canullo (1985) observed in Bailowieza Forest that a complex vegetation with many highly-competitive species quickly emerged on land, recently abandoned by agricultural practice and still rich in phosphate. The same could have occurred in Ename on the phosphate-rich, intensively-managed parcels reforested after 1916, where ancient-forest plant species may have had to cope with a dominance of competitive species. Similar negative effects of soil phosphate and nitrogen content on Anemone nemorosa cover have been cited by Pigott (1982). Corylus avellana seedlings also seem to have been excluded by highly competitive species. Overall, we may conclude that not only seed dispersal capabilities, but also, site quality parameters play an important role in the colonization process of the six indicator species. In the longer term, it can be expected that the impact of fringe relic presence on the distribution patterns of the species will wear out and soil phosphate content will be the more important residual affecting factor. 4.5. Colonization distances and rates There is scant information in the literature on colonization rates of ancient-forest plant species.

Rackham (1980) mentions colonization rates of ca. 100 m per century for Mercurialis perennis and Hyacinthoides non-scripta. Pollard (1973), on the other hand, indicates a rate of 10±30 m per century for Mercurialis perennis. Pigott (1982) records still lower ®gures of, respectively, 6±10 and 1±2 m per century for Hyacinthoides non-scripta and Anemone nemorosa. The variability of these ®gures may be partly explained by the lack of information in some of these studies on site quality, and the mentioned rates should not be compared as such. Our ®gures are situated somewhere within this range, with an average between 16 and 32 m per century and maxima between 28 and 55 m per century. Some literature sources make allusion to the possibility of relating information on the so-called seed dispersal shadow of the species with the shape of the colonization distance-frequency distributions or histograms (Harper, 1977; Willson, 1993). According to what is referred to as the `inverse square law' (Harper, 1977), steep slopes (steeper than ÿ2 on a logarithmic scale) of the regression function between the number of seeds and seed-dispersal distance, suggest that colonization occurs on an advancing continuous front, while ¯at slopes indicate a colonization pattern that is characterized by isolated outposts. Paris quadrifolia and Vinca minor exhibit unimodal colonization distance histograms symbolizing patchy distributions. The suggested rather ¯at slope of the seed dispersal shadow curve would lead us to conclude that seeds of these species are capable of bridging long distances from the source (the fringe relic) during colonization. Our ®eld data do not con®rm this. On the other hand, the inverse square law is valid for Mercurialis perennis, and Hyacinthoides non-scripta. Their monotonic distribution curves hint at steep seed-dispersal shadows and short seed-dispersal distances, which is con®rmed by our data. 5. Conclusion Research projects of this kind clearly identify some of the dif®culties nature management has to cope with in order to strive for high ecological values in newly established forests. In the short term, afforestation of set-aside farmland that was previously under intensive agricultural occupation will not result in ecologically

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valuable forest habitats (see also Peterken, 1993). The relatively immobile soil phosphate seems to represent a major barrier. The best chances for ecologically rich new forests arise on nutrient-poor relatively undisturbed sites. Because ancient-forest plant species cannot be considered mobile on a human-time scale, the integration of existing woody fringe relics at the periphery of new forests can be very effective. The assumption by Peterken and Game (1984) that, any new forest that incorporates some length of hedge will quickly have 10±20 forest plant species in its ground layer, is supported by our research. Any modeling exercise of plant dispersal at the landscape level faces site±quality problems. More data are needed about germination conditions and plant reproduction circumstances, and more research is necessary on the dispersal characteristics of these species. A profound understanding of their dispersal mechanisms is indispensable if the impact of global climatic changes is to be assessed at local and regional scales. Finally, these investigations have stressed the importance of historical and related habitat quality factors when attempting to unravel the colonization patterns of ecologically valuable forest plant species. While, historical ecology is invaluable for the study of forests as ecosystems with slow dynamics, it can, however, never be a surrogate for carefully planned ®eld observations and experiments. Acknowledgements We are very grateful to G. Tack and P. van den Bremt (Ministerie van de Vlaamse gemeenschap, Bestuur Monumenten en Landschappen, Gent) because they did a lot of the ®eld work and collected the historical data. We thank also to Hans Dufourmont for his help using the raster-cell oriented algorithms. G.F. Peterken and an anonymous reviewer provided an earlier manuscript of useful comments. References Aulakh, M.S., Doran, J.W., Mosier, A.R., 1992. Soil denitrification, significance, measurements and effects of management. Adv. Soil Sci. 18, 2±42. Bratton, S.P., 1994. Logging and fragmentation of broad-leaved deciduous forests: Are we asking the right ecological questions? Cons. Biol. 8, 295±297.

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