Regeneration dynamics of non-native northern red oak (Quercus rubra L.) populations as influenced by environmental factors: A case study in managed hardwood forests of southwestern Germany

Forest Ecology and Management 291 (2013) 144–153

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Regeneration dynamics of non-native northern red oak (Quercus rubra L.) populations as influenced by environmental factors: A case study in managed hardwood forests of southwestern Germany Kelly C. Major a,b, Peter Nosko a,⇑, Christian Kuehne c, Daniel Campbell b, Jürgen Bauhus c a b c

Department of Biology and Chemistry, Nipissing University, North Bay, Ontario, Canada P1B 8L7 Department of Biology, Laurentian University, Sudbury, Ontario, Canada P3E 2C6 Institute of Silviculture, Freiburg University, D-79085 Freiburg, Germany

a r t i c l e

i n f o

Article history: Received 5 September 2012 Received in revised form 4 December 2012 Accepted 6 December 2012 Available online 5 January 2013 Keywords: Gap ecology Introduced species Invasive species Quercus rubra Regeneration ecology Seedling growth

a b s t r a c t Quercus rubra L. (northern red oak), a tree species having moderate shade tolerance, is failing to regenerate across its native range in North America, largely due to its inability to compete with shade-tolerant species. Throughout central Europe, where it was introduced in the 18th and 19th centuries, Q. rubra exhibits prolific regeneration even when growing with shade-tolerant trees under closed canopy conditions. A better understanding of factors that allow the proliferation of Q. rubra in its adventive range may provide insights into the conditions necessary to promote Q. rubra in North America. Our study investigated the regeneration dynamics of Q. rubra in six hardwood stands near Freiburg, Germany in relation to site conditions and the relative abundance and growth of indigenous tree species in forest understoreys. Despite high (94–98%) canopy closure at all stands, the density of Q. rubra regeneration (<2 m in height) was greater than that of all other tree species combined, averaging 24 stems m1. Density of Q. rubra seedlings reached 125 stems m2 directly below seed trees; however, the lack of seedlings beyond 15 m from a seed tree suggested limited seed dispersal. Seedlings were less abundant at relatively fertile sites with lowest densities corresponding most closely to elevated soil calcium. The abundance of Q. rubra was most highly variable in the midstorey (trees and shrubs >2.0 m in height and <10 cm diameter at breast height) with densities ranging from 200 to 1500 stems ha1. Periodic selective harvesting at all stands, appears to maintain a disturbed state of mid-succession that allows Q. rubra seedlings to persist and recruit into the midstorey as canopy gaps become available. Clearly, stands of this non-indigenous species are successfully regenerating and the dominance of Q. rubra appears to be sustainable. Despite its benign performance in North America, Q. rubra can be an effective competitor under suitable conditions. Our findings deemphasize the importance of canopy closure on Q. rubra regeneration and suggest that in North America, preliminary cuts performed prior to shelterwood harvests should focus on midstorey removal of competitor species especially following oak mast years. Ó 2012 Elsevier B.V. All rights reserved.

1. Introduction Quercus rubra (northern red oak) is a mid-successional, midshade-tolerant hardwood tree that has considerable ecological and economic importance (Crow, 1988; Sander, 1990). Throughout eastern North America, forests dominated by Q. rubra are failing to regenerate (Crow, 1988). Widespread decline of this species corresponds to several decades of regenerative failure (Lorimer, 1984; Crow, 1988; Lorimer et al., 1994) attributed primarily to fire suppression and the resulting decrease in disturbance frequency (Nowacki et al., 1990). On most sites, Q. rubra regeneration is primarily regulated by light (Crow, 1988; Lorimer et al., 1994; Dech ⇑ Corresponding author. Tel.: +1 (705) 474 3450x4323; fax: +1 (705) 474 1947. E-mail address: [email protected] (P. Nosko). 0378-1127/$ - see front matter Ó 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.foreco.2012.12.006

et al., 2008). Periodic fires reduce understorey competition and create an appropriate light environment in which Q. rubra seedlings can re-sprout and grow (Abrams, 1992; Huddle and Pallardy, 1999). In the absence of fire, shaded conditions persist allowing more shade-tolerant (yet less fire-adapted) tree species to recruit into Q. rubra stands and produce dense understoreys that further suppress oak regeneration and eventually replace the canopy as gaps become available (Lorimer, 1984; Pallardy et al., 1988; Abrams, 1996; Aldrich et al., 2005). The harvest of Q. rubra stands often expedites this stand conversion which is counteracted with a combination of shelterwood harvesting (to approximately 60% of the original basal area) and understorey tending (Loftis, 1990; Brose et al., 1999; Van Lear, 2004). Together, these laborious and expensive techniques increase the likelihood of, but do not guarantee, successful regeneration of Q. rubra after harvest.

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In contrast, Q. rubra has been readily regenerating in central Europe since its early 18th century introduction (Timbal, 1994; Magni Diaz, 2004; Vor, 2005) despite a near total absence of fire (Tinner et al., 2005). Although its wood has traditionally been considered of lesser value compared to that of native European oaks, Q. rubra was found to grow up to 60% faster than Q. robur L. and Quercus petraea Liebl. (Magni Diaz, 2004; Vansteenkiste et al., 2005). As the European forest industry intensified in the early 19th century, Q. rubra was actively introduced onto the landscape to improve timber yields (Kenk and Borsy, 1994; Magni Diaz, 2004). These practices continued into the 21st century, and Q. rubra is now naturalised throughout western and central Europe (FAO, 2009; GBIF, 2009). Q. rubra remains economically important in several European countries; however, recent efforts to promote declining European oak species, in combination with rising opposition to the proliferation of non-indigenous plants, is causing controversy over its continued industrial use (Reinhardt et al., 2003; Magni Diaz, 2004). In Poland, Q. rubra has been identified as one of that country’s most invasive plants as it is recruiting extensively into nature reserves and is thought to be threatening native biodiversity (Chmura, 2004; Chmura and Sierka, 2005). In Belgium, government initiatives are attempting to eradicate Q. rubra from Flemish forests (Vansteenkiste et al., 2005). Q. rubra has been reported by the German Federal Ministry of the Environment to hinder natural forest succession and impair native plant and animal communities (Reinhardt et al., 2003). The apparent discrepancy in the regenerative capacity of Q. rubra in North America and Europe raises questions of how a species experiencing widespread regenerative failure and requiring intensive management within its native range can so successfully regenerate with little or no intervention in an introduced range. Uncharacteristically vigorous growth and reproduction of nonindigenous populations of otherwise benign plant species is a well-documented, but not fully understood phenomenon (Mack et al., 2000). A high degree of vigour in an alien plant is frequently cause for concern as it can increase the invasiveness of a plant and facilitate its spread in an introduced range. An instance where a valuable species is in decline across its native range yet exhibits vigorous growth abroad provides a unique opportunity to study the conditions under which the species thrives. To date, few studies have assessed the regeneration ecology of Q. rubra in Europe, especially in managed forests (Vor, 2005) and none have attempted to apply such observations to improve North American management practices. Considering the widespread regeneration failure of Q. rubra in its native range and the limitations that physical, chemical and biotic factors can impose on successful regeneration, the objectives of our study were to address the following questions: (1) in the adventive range, how does the abundance of regenerating red oak compare with that of native tree species under high canopy closure; (2) how does the degree of natural regeneration of Q. rubra in central Europe relate to physical, chemical and biotic site factors; and (3) what specific site factors in the non-native range contribute to the successful regeneration of Q. rubra? Such insights could provide strategies to promote the regeneration of Q. rubra forests in the native range and if necessary, control the regeneration and spread of nonindigenous populations.

2. Methods 2.1. Site description This study was conducted in vicinity of Freiburg im Breisgau (Freiburg), in southwestern Baden-Württemberg, Germany (48°000 N, 07°510 E) (Fig. 1). Freiburg has a mean annual tempera-

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ture of 11 °C, mean January and July temperatures (coldest and warmest months) of 0.9 °C and 19.3 °C, respectively, 177 days per year above 10 °C and a mean annual precipitation of 760 mm (Bläsing, 2008). In a North American context, this is comparable to climatic conditions near the 40th degree north latitude in the eastern United States (e.g. Illinois, Indiana and Ohio). The climate of Freiburg also coincides closely with the mean annual temperature (11.5 °C) and precipitation (1045 mm) within the native range of Q. rubra (Rey, 1960). Six Q. rubra stands were selected among three local forest districts; the North Mooswald (stands 1 and 2), South Mooswald (stands 3 and 4), and the Rosskopf (stands 5 and 6) (Fig. 1). Stand selection was based on: (1) the presence of Q. rubra in the overstorey; (2) the absence of observable abnormalities uncharacteristic of the surrounding forest; (3) interspersion and (4) accessibility. The North and South Mooswald were both lowland forests situated in the former floodplain of the Dreisam River. Soils are a gleyic cambisol (FAO, 1998) comprised of a loess layer of varying thickness over alluvial silicate gravel (Villinger, 2008). These soils have a sandy texture and are generally well drained throughout the summer and fall but can become periodically waterlogged in the winter and spring (Hügin, 1990). Both Mooswald forests are comprised primarily of mixed hardwood stands frequently dominated by Q. robur L. (pedunculate oak) and Carpinus betulus L. (hornbeam) with varying amounts of Acer pseudoplatanus L. (sycamore maple), Acer platanoides L. (Norway maple), Fraxinus excelsior L. (European ash), Betula pendula Roth. (silver birch), Tilia cordata Mill. (smallleaved lime) and Tilia platyphyllos Scop. (large-leaved lime). Stands of Q. rubra were situated throughout both forests, with this species achieving high dominance in some areas. Stands 1 through 4 ranged in elevation from 220 to 230 m ASL. The Rosskopf is an upland forest located on a hillside with a predominantly westward aspect. Soils are a loamy cambisol formed from a gneissic parent material and mixed with loess (FAO, 1998). Canopy tree species included Q. rubra, Fagus sylvatica, Acer spp., C. betulus and Q. robur. Stand 5 was situated at 300 m ASL on a 20% northwest facing slope while Stand 6 was at 380 m ASL on a 27% southwest slope. Stands observed in this study were of a similarly age; 41– 56 years. They were established shortly after the Second World War by planting efforts that made use of Q. rubra. In this region, C. betulus and Tilia spp. were commonly planted as trainer species with Q. rubra to reduce epicormic branching in the latter; however, it is unclear whether C. betulus and Tilia spp. were planted at the specific stands described in this study or whether their current presence resulted from natural regeneration. Since establishment, crown thinning has regularly occurred at all stands using single tree selection approximately once or twice a decade. In addition, the salvage of downed woody debris by permit is commonly practiced in this region. 2.2. Field sampling At each of the six stands, three systematically positioned 50  50 m blocks were established. Blocks were spaced at least 10 m apart and were at least 10 m from any road or clearing. Reduced size of the two Rosskopf stands permitted only 30  30 m blocks and required reduced spacing between blocks. Four or five randomly placed 2  2 m plots were located in each block producing 75 plots across 18 blocks at six stands. All measurements were made during July and August 2009. A composite soil sample of eight evenly distributed cores from the top 15 cm of mineral soil was collected from each plot. All soil samples were collected on the same day during an interval of overcast yet precipitation-free weather, permitting relative comparisons of soil moisture content (% dry weight). Soil samples were

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Fig. 1. Location of the six study stands (j) within three forests, the North Mooswald, South Mooswald and Rosskopf, near Freiburg, Germany (star).

also chemically analysed for pH, total nitrogen (N), sodium bicarbonate extractible phosphorus (P), and ammonium acetate extractable potassium (K), magnesium (Mg) and calcium (Ca). All chemical analyses were performed by Guelph University Laboratory Services in Guelph, Ontario. Canopy closure was estimated at 2.0 m above the forest floor of each plot with a spherical densiometer (Lemon, 1956). Stand structure was described according to three strata; the understorey (cover of all plants <2 m in height), the midstorey (trees and shrubs >2.0 m in height and <10 cm diameter at breast height; DBH) and the overstorey (trees with DBH P 10.0 cm). The delineation of our stands into these strata was similar to that used by Lorimer et al. (1994) and Dech et al. (2008). The structure and composition of the midstorey and overstorey was assessed by performing point-quarter surveys (Cottam and Curtis, 1956) for each block (n = 3 per stand) using the centers of each of the 75 plots as points. The midstorey was quantified for stem density per hectare and the overstorey by Stand Density Index (SDI) (Reineke, 1933) which expresses the density (stems ha1) that an overstorey would have to have for its quadratic mean diameter to be set to 25 cm. The distance from each plot center to the nearest mature (P10 cm DBH) Q. rubra tree was recorded as a measure of seed tree proximity. The composition and abundance of species in the understorey plant community (<2 m) was assessed and quantified at each plot by assigning cover values to all vascular plants according to the midpoints of a modified standardized scale (Daubenmire, 1968; Dech et al., 2008) of seven cover classes; 0–5%, 6–15%, 16–25%, 26–50%, 51–75%, 76–95% and 95–100%. Bryophyte cover was estimated as a functional group (total bryophyte cover). Shannon diversity (H0 ) and mean Ellenberg Indicator Value for Light (EIVL) (Ellenberg, 1988) were calculated, with the latter weighted according to species cover values. As a non-indigenous species, Q. rubra was not classified by Ellenberg (1988) and subsequently could not contribute to EIV-L calculations. All Q. rubra seedlings in the understorey were counted and measured for height and basal diameter. Total seedling density (stem m2) was calculated for Q. rubra and all other tree species. Nomenclature for all North American and European species follows Gleason and Cronquist (1991) and Tutin et al. (1964–80), respectively.

2.3. Data analyses Environmental variation within and among stands was investigated with a principal components analysis (PCA) using PC-ORDÒ for Windows, Version 5.31 (McCune and Mefford, 1999). All plot, block and stand data (soil chemistry and moisture, total understorey cover, Shannon diversity, EIV-L, distance to nearest seed tree, canopy closure, midstorey stem density, overstorey SDI, and years since the previous selective cut) were included in the PCA. Axis (principal component) significance was assessed with randomisation tests of 999 iterations. Model loadings were plotted in relation to significant axes via vectors radiated from the centroid of the ordination scores and depicted the direction of incline and relative strength of each included variable. Only loadings with significant Pearson correlations to one or both plot axes were included (McCune and Grace, 2002). A series of forward stepwise multiple regressions was used to isolate environmental variables controlling Q. rubra regeneration (Field, 2005). The mean density, height and diameter of Q. rubra seedlings in each plot (dependent variables) were logarithmically transformed to normalise residuals. Plots with no oak regeneration required removal from height and diameter analyses to satisfy normality (n = 70 for these two dependant variables). All soil and stand properties, with the exception of EIV-L, were included as independent variables. To linearise relationships, all soil nutrient data were logarithmically transformed prior to statistical analysis. EIV-L was excluded from regression analysis due to shared co-linearity with other measured variables. Regression analyses were completed using SPSS Statistics 17.0 (SPSS, 2007) with relationships being considered significant at p < 0.05. Because plots are nested within blocks then within sites, individual plots may not actually be independent. Multiple regressions may therefore exaggerate the actual Type I error rates; however, they allow an exploration of causal mechanisms for the differential success of red oak.

3. Results In the understorey, the density of Q. rubra seedlings was generally high at all stands; averaging 24 stems m2

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K.C. Major et al. / Forest Ecology and Management 291 (2013) 144–153 Table 1 Growth variables (mean ± SD) for regenerating (<2 m) Quercus rubra and other tree speciesa in the understorey of six Q. rubra stands near Freiburg, Germany. North Mooswald

South Mooswald

Rosskopf

Stand 1

Stand 2

Stand 3

Stand 4

Stand 5

Stand 6

Q. rubra Frequency (%) Density (stems m2) Height (cm) Diameter (mm)

100 32.6 ± 20.5 23.0 ± 5.9 2.3 ± 0.5

83.3 31.8 ± 36.6 15.4 ± 7.4 1.9 ± 0.9

93.3 13.0 ± 12.7 31.3 ± 33.0 2.9 ± 1.8

100 60.6 ± 46.5 22.7 ± 10.7 2.65 ± 0.9

91.6 1.7 ± 1.9 22.7 ± 18.2 2.6 ± 1.7

66.7 4.2 ± 3.6 10.9 ± 8.3 1.4 ± 1.1

Other tree species Density (stems m2)

1.1 ± 2.8

6.5 ± 8.0

7.7 ± 17.5

0.8 ± 1.4

0.1 ± 0.4

2.1 ± 3.0

a

Other tree species (in descending order of importance) include Carpinus betulus, Acer pseudoplatanus, Fraxinus excelsior, Q. robur, A. platanoides, Tilia cordata, T. platyphyllos and Fagus sylvatica.

(240,000 stems ha1) and outnumbering that of all other tree species combined (Table 1). Within stands, the distribution of Q. rubra seedlings was patchy yielding densities within plots that ranged from 0 to 125 stems m2. Among stands, seedlings were more abundant in the lowland stands of the North and South Mooswald (averages ranging from 13.0 to 60.6 stems m2; Table 1, Fig. 2) than the upland Rosskopf (1.7 and 4.2 stems m2; Table 1). The combined density for seedlings of all other tree species averaged 3.2 stems m2, and was lower than the density of Q. rubra seedlings in 85% of plots. Midstorey stem density was the greatest source of architectural variation among the six stands. The density of saplings and midstorey trees in this middle stratum ranged from 200 stems ha1 at stand 1 of the North Mooswald to a high of 1500 stems ha1 in both Rosskopf stands (Table 2). The resulting variation in stand stratification caused an observable gradient of light availability at the forest floor. In the North and South Mooswald, the lack of dense midstoreys occasionally produced a park-like stand structure (Fig. 3). EIV-L derived from the North Mooswald suggested plant communities adapted to relative light levels greater than 50% (Table 1). The Rosskopf had the densest midstorey and an EIV-L indicative of communities adapted to shaded environments of between 5% and 50% relative light. PCA of all measured environmental variables yielded three significant axes that together explained 60% of the total variance. The resulting ordination plots (Fig. 3) separated study plots according to intra-stand and inter-stand variation. Soil chemistry (Ca, Mg, K, P and pH) drove microsite (inter-stand) variation along principal component 1 (27% variation) but varied more within stands than

Fig. 2. Dense Quercus rubra seedlings in the understorey of stand 3 (South Mooswald), near Freiburg, Germany.

among them. Greatest nutrient concentrations were observed at stand 6 where one block (four plots) was located in a forested area that likely received nutrient input from past agricultural activity that ended in 1975 (Table 2). Principal component 2 (22%) largely corresponded to inter-stand variation, separating upland from lowland stands with extremities defined by the North Mooswald and the Rosskopf. Lowland stands had greater soil moisture, total soil N and total understorey plant cover (excluding Q. rubra) as well as reduced overstorey SDI compared to upland stands (Table 2). The greater understorey cover in the lowlands resulted from dense colonies of the sedge Carex brizoides which achieved mean covers of 80% and 50% at stands 1 and 2 in the North Mooswald and exceeded 95% cover on some individual plots (Fig. 4). Proximity to a seed tree also correlated strongly to both the first and second PCA axes reflecting variability within and among stands. Principal component 3 (11%) further separated plots by disturbance history, with more recently thinned stands having a reduced overstorey SDI and greater Shannon diversity. All stands had high canopy closures (means >90%), yet intermittent canopy gaps occasionally produced higher light microenvironments with closures as low as 78%. These gaps were more frequent, yet still generally sparse, at recently thinned stands resulting in a correlation between canopy closure and principal component 3. Stepwise multiple regression revealed that variables of soil chemistry, stand structure and thinning history accounted for 75% of the total variation in the density of Q. rubra seedlings (Table 3). These included, in decreasing order of importance, soil calcium, years since thinning, overstorey stand density index, distance to seed tree and, to a lesser extent, tall understorey density and low understorey density. With the exception of total N, Q. rubra seedlings were denser at lower soil nutrient concentrations and corresponded most closely with soil Ca. Soil Ca correlated significantly to soil pH, K, P and Mg (positive) as well as total N (negative). All soil nutrient variables were entered into the stepwise regression; however, because of shared colinearity, only soil Ca was used since it best explained the dependant variable (yielded the highest r2). Only four seedlings were observed at Ca concentrations exceeding 500 mg L1 and only one above 800 mg L1. Ca concentrations were consistently highest in the nutrient enriched block of stand 6, where Q. rubra was entirely absent from the understorey. The density of Q. rubra seedlings was greatest in stands that had recently undergone selective cutting. In the North and South Mooswald, Q. rubra seedlings were abundant at all stands, but seedling density was nearly five times greater at stands thinned 2 years prior to this study than those thinned 6 years before the study. The same trend was observed in the Rosskopf; stand 6, thinned 6 years after stand 5, had 2.5 times more Q. rubra seedlings. The density of Q. rubra seedlings was strongly related to distance from a seed tree. Seedling density was greatest immediately below seed tree boles and decreased with distance from the tree.

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Table 2 Soila and stand properties (mean ± SD) of six Quercus rubra stands near Freiburg, Germany. North Mooswald

a

c d

Rosskopf

Stand 1 14

Stand 2 12

Stand 3 14

Stand 4 12

Stand 5 12

Stand 6 11

Soil properties pH (median) N P K Ca Mg Moisture (%)

4.00 0.45 ± 0.06 15.4 ± 4.4 63.8 ± 9.1 107 ± 51.9 41.6 ± 9.2 26.9 ± 6.2

4.15 0.38 ± 0.11 10.4 ± 3.2 62.8 ± 9.7 162 ± 72.5 45.7 ± 13.6 21.2 ± 6.6

4.00 0.27 ± 0.07 11.0 ± 3.8 58.0 ± 17.9 136 ± 84.0 53.4 ± 30.8 14.2 ± 4.7

3.85 0.21 ± 0.04 8.3 ± 2.4 42.8 ± 6.1 154 ± 126.6 62.8 ± 39.7 11.5 ± 3.1

4.10 0.19 ± 0.02 13.1 ± 5.1 71.8 ± 16.1 383 ± 588.6 52.6 ± 18.2 18.1 ± 3.2

4.20 0.17 ± 0.03 22.2 ± 25.0 92.6 ± 34.0 638 ± 735.2 142.5 ± 145.6 8.1 ± 1.0

Stand properties Years since thinning Canopy closure (%) Distance to seed treea (m) Overstorey SDIb (stems ha1) Midstorey density (stems ha1) Total understorey coverc (%) Shannon diversity (h) Weighted EIV-Ld

5 95.6 ± 4.9 4.0 ± 2.3 439 ± 95.4 193 ± 23.9 85.0 ± 21.3 1.2 ± 0.4 5.5 ± 0.6

4 96.8 ± 2.9 7.0 ± 5.7 473 ± 146.8 430 ± 28.0 71.4 ± 37.7 1.6 ± 0.3 4.8 ± 0.3

6 96.5 ± 4.4 10.5 ± 6.7 441 ± 135.4 602 ± 376.1 24.3 ± 23.9 1.6 ± 0.5 4.5 ± 0.8

2 93.9 ± 6.4 2.8 ± 2.0 484 ± 91.7 885 ± 189.8 52.1 ± 58.6 1.4 ± 0.7 4.5 ± 0.5

8 98.3 ± 1.3 3.1 ± 1.3 770 ± 129.4 1516 ± 183.3 49.4 ± 27.0 1.5 ± 0.3 4.3 ± 0.5

2 97.5 ± 2.1 7.5 ± 8.0 784 ± 90.6 14476 ± 1008.1 47.9 ± 42.3 1.4 ± 0.5 4.2 ± 0.5

N

b

South Mooswald

Units for concentration of total N is % and mg L1 for the extractable fraction of all other elements. SDI = Stand density index. Sum of all plant cover excluding Q. rubra. EIV-L = Ellenberg Indicator Value for Light.

This contributed to the patchy distribution of seedlings observed at all stands in this study and only six seedlings were observed beyond 15 m from a seed tree. Overstorey SDI was also negatively associated with seedling density, as was the density of the midstorey and total understorey cover. The height of Q. rubra seedlings in all stands was generally below 50 cm. Collectively, canopy closure, thinning history and Shannon diversity explained 36% of the observed variation in mean seedling height (Table 3). The height of Q. rubra seedlings generally increased as canopy closure decreased indicating superior growth under canopy gaps. In the absence of a dense midstorey, canopy gaps in the North and South Mooswald allowed seedlings to grow unimpeded from the understorey into dense midstorey thickets (Fig. 5). Seedling heights were also greater as time since previous thinning increased. In the North Mooswald, a 1 year disparity was associated with 50% greater mean height at stand 1 than stand 2 (Table 1). The same was observed in the South Mooswald where a 4 year difference between the time that stands 4 and 3 were thinned was associated with 40% greater height. In the Rosskopf, Q. rubra seedlings were twice as tall, on average, at stand 5 than stand 6; corresponding to a 6 year difference in time since thinning. Q. rubra seedling height was also inversely related to Shannon diversity (Table 3). Mean seedling diameters increased as canopy closure decreased and time since thinning increased; these two variables accounting for 24% of the variation in diameter of red oak seedlings (Table 3).

4. Discussion By North American standards, the abundance of Q. rubra in the understorey of hardwood forests around Freiburg was exceptional; often resulting in a dense carpet-like cover of seedlings. Seedlings of this species outnumbered those of all other tree species combined and achieved densities far greater than in Q. rubra stands in North America. Steiner et al. (1993), who compared oak stands within native (Pennsylvania) and introduced (France) ranges found that in Pennsylvania, mean densities of Q. rubra seedlings ranged from 0.01 to 0.87 stems m2; values consistent with observations

of Q. rubra populations throughout Eastern North America (Nowacki et al., 1990; Goebel and Hix, 1996; Dech et al., 2008). In France, Steiner et al. (1993) observed near-continuous carpets of Q. rubra seedlings with densities ranging from 21 to 40 stems m2, similar to densities in our lowland stands (North and South Mooswald). While Q. rubra was far less prolific in our upland forests, the lowest mean density observed in the upland Rosskopf (1.7 stems m2; stand 5) was still double the highest seedling density observed in Pennsylvania by Steiner et al. (1993). In a comparison of Q. rubra regeneration in three forested locations in Germany, Vor (2005) measured a maximum Q. rubra density of 80 seedlings m2 and a mean density of 20 seedlings m2 in a relatively warm, dry and nutrient-poor stand that had no grazing by deer. These data together with our maximum seedling densities that exceeded those reported by Vor (2005), suggest an abundant reservoir of advanced regeneration and is a strong indication that Q. rubra populations in Europe are sustainable and that their dominance is likely to be maintained following harvest of overstorey trees (Carvell and Tryon, 1961; Steiner et al., 1993). Ordination analysis of the abiotic and biotic environment provided insight into Q. rubra regulation at two scales; smaller intrastand variation and larger inter-stand variation, with the latter resulting in a clear differentiation between lowland and upland stands. The degree of Q. rubra regeneration varied greatly at both of these scales. PCA indicated that Q. rubra regeneration was optimal at lower soil nutrient (P, K, Mg and Ca) concentrations. Q. rubra is a stress tolerant species that remains relatively unresponsive to reduced soil fertility (Crow, 1988; Kolb et al., 1990; Colin-Belgrand, 1994). Instead, greater declines in the growth and vigour of less stress–tolerant competitors frequently provide regenerating Q. rubra with a competitive advantage on less fertile soils (Crow, 1988; Kolb et al., 1990; Major, 2008). Regression analysis confirmed this optimization and indicated that soil Ca content was the soil nutrient most strongly associated with Q. rubra density. In the top 15 cm of soil, the concentration of Ca varied to a greater degree than that of any other measured nutrient, with concentrations sometimes differing by an order of magnitude within a single stand. The detection of Ca as the strongest nutrient predictor of Q. rubra density may simply reflect the breadth of our observed concentrations; however, the intolerance of Q. rubra seedlings of

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Fig. 3. Ordination bi-plots depicting the first three axes derived from principal components analysis of the biotic and abiotic environment in 75 experimental plots in six Quercus rubra stands in the vicinity of Freiburg, Germany. For clarity, the plots have been divided according to stand (A and B), significant loadings (Pearson correlations p 6 0.05) (C and D) and the density of Q. rubra regeneration (<2 m) (E and F). Loadings arrows indicate the direction and relative strength of environmental gradients relative to the axes. Points are scaled to reflect Q. rubra seedling density. Environmental variables include years since thinning (TY), distance to nearest Q. rubra seed tree (ST), overstorey SDI (OS), midstorey stem density (MS), total understorey cover (US), Ellenburg Indicator Value for light (EL), Shannon diversity (SH), as well as the soil variables; moisture content (MO), pH (pH), total nitrogen (N), and logarithmically transformed calcium (Ca), magnesium (Mg), potassium (K), and phosphorus (P).

high concentrations of Ca is well documented (Timbal and Dewilder, 1994). Gelpe et al. (1986) demonstrated that the regular application of CaCO3 solution as dilute as 1% to forest soils resulted in a 70% mortality of greenhouse grown Q. rubra seedlings after 1 year; compared to 8% mortality without added CaCO3. Timbal and Gelpe (1989) further demonstrated that elevated Ca concentrations are most detrimental to seedling growth and survival in the top 30 cm of soil. In our study, few Q. rubra seedlings were observed at Ca concentrations exceeding 500 mg L1, which may suggest that this value approximates an upper threshold of Q. rubra seedling tolerance in Freiburg. In central Europe, where Q. rubra is sometimes considered invasive and so ‘‘aggressive’’ that eradication programs have been proposed (Vansteenkiste et al., 2005), future research could investigate the effectiveness of Ca additions through liming as a control agent. However, studies in Pennsylvania by Long et al. (2012), showed that height and diameter growth of Q. rubra seedlings was unresponsive to three levels of dolomitic limestone for a period of 6 years following application. Comparing all stands, the density of Q. rubra in the understorey was quite variable. In the North and South Mooswald, Q. rubra

seedlings formed dense mats directly below mature Q. rubra boles; generally seedling density decreased with increased distance from a seed tree. The same was observed in the Rosskopf, but with lower total seedling densities. García and Houle (2005) observed patchy distributions of Q. rubra seedlings in southern Quebec and reported that the density of Q. rubra seedlings was most strongly influenced by proximity to a seed tree and directness of seed deposition. Vor (2005) noted that evidence of Q. rubra regeneration in Germany was scarce beyond 50 m from a seed source and suggested that Q. rubra dispersal is limited. In our study, few seedlings were observed beyond 15 m from a seed tree, supporting Vor’s (2005) observations and contrasting with reports from Poland that Q. rubra is in a state of range expansion and is recruiting into protected nature reserves suggesting that seed dispersal is not limited (Chmura, 2004; Chmura and Sierka, 2005). Low seed dispersal in German forests suggests a lack of seed predation (Vor, 2005) which likely contributes to the formation of dense seedling banks. Regularity of acorn production in European populations might also contribute to the hyper-abundance of Q. rubra regenerating directly adjacent to seed sources. Anecdotal but undocumented

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Fig. 4. Sparse midstoreys observed throughout North and South Mooswald forests of Freiburg, Germany, frequently resulted in a park-like stand structure with dense sedge (Carex brizoides) cover as shown for stand 1.

Fig. 5. Quercus rubra saplings in the vicinity of a canopy gap in the South Mooswald (stand 3) growing directly from the understorey into a dense thicket entering the midstorey.

observations by local foresters suggest that Q. rubra populations in Freiburg mast more frequently than those in the native range where Q. rubra stands generally produce seed crops on 2–5 year cycles (Sander, 1990). All stands observed in this study have been managed by periodic selective thinning; a moderate and frequent anthropogenic disturbance that strongly influences stand structure and plant community composition (Thomas et al., 1999; Decocq et al., 2004, 2005; Calster et al., 2008). While all stands had generally closed canopies, the regularity with which these forests are being thinned appears to result in the maintenance of a regularly disturbed understorey that is preventing the development of a steady state (Carvell and Tryon, 1961; Aude and Lawesson, 1998). In France, Chabrerie et al. (2008) observed that a similar ‘‘management-sustained non-equilibrium’’ was promoting the invasion of the North American tree Prunus serotina Ehrh. (black cherry) by keeping the plant community and environment in a state of disruption and by releasing P. serotina seedlings from suppression. This also appears to be occurring in the forests surrounding Freiburg favouring the disturbance tolerant and mid-successional Q. rubra and resulting in greater seedling densities at the more recently thinned stands (Carvell and Tryon, 1961). Forgoing the selective harvest of stands dominated by Q. rubra (i.e. decreasing

disturbance frequency and maintaining closed canopies) in this region may allow for the successional replacement of this species as observed in North America; although a better understanding of the shade tolerance of Q. rubra relative to local tree species is needed. The scarcity of the midstorey across the lowland and resulting park-like forest structure strongly contrasts with observations from oak stands throughout North America. Nowacki et al. (1990) surveyed 46 Q. rubra stands in Wisconsin and observed midstoreys averaging 1700 to 3340 stems ha1. Moreover, Goebel and Hix (1996) demonstrated that young oak stands are prone to greater stratification than older ones. From their survey of 42 mixed oak stands in Ohio, the youngest age class (70–89 years) had the densest midstoreys, averaging 3000 stems ha1 (all species). No age class averaged below 1600 stems ha1. All stands observed in our study were under 60 years of age, yet no stand had a midstorey exceeding 1550 stems ha1. The cumulative average of all our lowland stands (ca. 500 stems ha1) represents one-sixth of the density of all midstorey species that would otherwise be expected in a similarly aged North American stand. Light suppression is the primary source of growth regulation of Q. rubra seedlings (Phares, 1971; Canham et al., 1996; Dey and Parker, 1997) and the development of dense shade-tolerant understoreys below oak canopies is the primary cause of the regenerative failure characteristic of North American oak decline (Crow,

Table 3 Stepwise multiple regression analysis of environmental (predictor) variables on the response variables of density, height and diameter of Quercus rubra in the understorey. Logarithmic transformations were applied to satisfy residual normality. N = 75 for density; N = 70 for height and diameter. Cumulative r2 values and unstandardized coefficients (b values) are reported for each significant predictor. b

SE b

p

Constant Log 10 soil Ca Years since thinning Overstorey SDIa Distance to seed tree Midstorey density Understorey cover

0.38 0.49 0.55 0.67 0.70 0.75

3.651 0.388 0.090 0.001 0.061 <0.001 0.004

0.270 0.140 0.019 <0.001 0.009 <0.001 0.001

<0.001 0.007 <0.001 <0.001 <0.001 <0.001 0.001

Constant Canopy closure Years since thinning Shannon diversity

0.21 0.30 0.36

3.470 0.022 0.030 0.081

0.412 0.004 0.009 0.035

<0.001 <0.001 0.002 0.025

Constant Canopy closure Years since thinning

0.19 0.24

1.575 0.011 0.011

0.247 0.003 0.005

<0.001 <0.001 0.042

Predictor

log10 Density

log10 Height

log10 Diameter

a

r2

Variable

SDI = Stand density index.

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1988). In Wisconsin, the experimental removal of dense (P3000 stems ha1) tall understoreys from two mixed-oak stands resulted in a 10- and 140-fold increase in oak (Q. rubra and Q. alba) seedling densities over 5 years despite the retention of a closed (86%) canopy (Lorimer et al., 1994). This treatment also resulted in a threefold increase in the survivorship of artificially planted Q. rubra seedlings over the same period (Lorimer et al., 1994). Where present, shading from the midstorey at our stands appeared to reduce Q. rubra density in the understorey. However, mean midstorey densities in the North and South Mooswald that were 80% and 50% lower, respectively, than in the Rosskopf, corresponded to Q. rubra understorey densities that were 11 and 13 times greater. This indicates that while the canopy was generally closed in all stands, light penetration to the forest floor was facilitated by the lower density of the midstorey, maintaining improved light microenvironments that are associated with more vigorous Q. rubra seedling growth and reduced mortality (Phares, 1971; Timbal and Dreyer, 1994; Stringer, 2006). This light gradient from the Rosskopf to the North Mooswald was confirmed by a shift in species composition toward less shade-tolerant assemblages (decreased EIV-L; Ellenberg, 1988). Our European sites had a high degree of canopy closure where regenerating Q. rubra occurred in the presence of relatively shade-tolerant (Niinemets and Valladares, 2006) canopy trees such as C. betulus, A. platanoides, A. pseudoplatanus and T. cordata. Under these conditions, Q. rubra regeneration was evident on 90% of our plots and formed the tallest stems in 80% of cases. This suggests that light limitations and competitive disadvantages under shade are not as pronounced as observed in similar situations in North America. The range of Q. rubra in Europe is not well defined; however, it is likely that Freiburg is situated in the southern portion of this range. The latitude of Freiburg would place this location beyond the northern limit of Q. rubra in North America. Given the relatively high latitude of the European range compared to the native North American range, Q. rubra populations in Europe would be exposed to greater day lengths over the growing season. Furthermore, at comparable latitudes, locations in Europe tend to have milder climates than those in eastern North America. European populations of Q. rubra could benefit from a greater photoperiod, and a growing season that begins sooner than in the native range. Higher air temperatures at a time of relatively long days in the early growing season could play a significant role in the success of Q. rubra in Europe. Stand origin may also contribute to this success. In North America, most red oak stands are the result of natural regeneration following disturbance and are characterised by several overstorey species and understoreys typically having a dense cover of shrubs and herbaceous plants. Partial harvest of canopy trees or natural gap formation can stimulate rapid growth of understorey plants and lead to understory shade levels that are similar to those imposed by the original canopy (Dech et al., 2008). The goal of promoting oak in managed forests necessitates control of competing vegetation in the understorey. In central Europe where fire disturbances are rare, existing Q. rubra stands were largely planted and may have started with fewer species capable of displacing Q. rubra in the understorey. Q. rubra seedling density was negatively related to total plant cover in the understorey, although causality in this relationship is unclear. Steiner et al. (1993) observed a similar relationship in France which they attributed to a rather continuous ‘‘canopy’’ of Q. rubra seedlings competitively excluding native herbaceous plants. With densities as high as 125 stems m2 observed in our study exceeding those reported for France, it is probable that Q. rubra seedlings are imposing intense above- and belowground competition resulting in a similar exclusion of local plant species in Freiburg. Unlike Steiner et al. (1993), we cannot conclude that the causality of the relationship is strictly one-way. Like Carvell

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and Tryon (1959), we observed greater understorey plant cover at relatively moist stands, but in the form of dense graminoid cover composed primarily of C. brizoides. This sedge invades managed stands and is a good indicator of the extent to which the North and South Mooswald forests have been influenced by repeated human induced disturbance (Dzwonko, 1993; Thomas et al., 1999; Decocq et al., 2004; Chmura and Sierka, 2007). Dense colonies of C. brizoides do not compete for light, but instead provide strong belowground competition that can reduce the germination and growth of other plants, including shrubs and trees (Dzwonko, 1993; Dzwonko and Gawron´ski, 1994; Falin´ski, 1998). Competition due to a dense cover of graminoids has been shown to significantly reduce Q. rubra seedling growth and biomass allocation to shoots but that the detriment to oak is partially mitigated relative to other tree species (e.g. Liriodendron tulipifera L.) by oak’s larger seed size and production of an extensive initial root base (Kolb and Steiner, 1990). The North and South Mooswald, areas with a dense cover of C. brizoides, generally had a low density of Q. rubra seedlings suggesting that while Q. rubra may competitively exclude some native species, oak seedlings also experience a reduction in density in the presence of dense graminoid cover. It is probable, however, that competition with C. brizoides is less detrimental to the vigour of Q. rubra seedlings than to those of native tree species, the majority of which are anemochorous (e.g. C. betulus, Acer spp., Tilia spp. and F. excelsior) having sacrificed seed size for increased dispersal (Kolb and Steiner, 1990). In this way the suppressive influence of C. brizoides, while perhaps directly detrimental to the growth of Q. rubra seedlings, could indirectly offer an overall competitive advantage to oak by reducing aboveground competition with other plant species and potentially contributing to the park-like stand structure (Kolb et al., 1990; Kolb and Steiner, 1990). The heights and diameters of Q. rubra seedlings were greatest in the vicinity of canopy gaps where light availability was relatively high. Although the frequency of canopy gaps was greatest immediately following a selective thinning and gradually decreased over time, the height of Q. rubra seedlings was positively related to the time since thinning, denoting an initial pulse of seedling recruitment following harvest that would then proceed to grow. While the majority of seedlings were relatively low in stature, heights were greatest under persistent canopy gaps and those produced by wind-throw in the years after thinning. The formation of canopy gaps can release Q. rubra seedlings from suppression, improving their growth and vigour (Naidu and DeLucia, 1997, 1998). In North American forests, dense heterospecific midstoreys frequently prevent light penetration to the forest floor, inhibiting midstorey recruitment of Q. rubra seedlings in favour of more shade-tolerant species (Barden, 1981; Beckage et al., 2000; Cowell et al., 2010). In contrast, the lowland stands observed in this study had sparse midstoreys that, in the presence of a gap, permitted Q. rubra seedlings to form dense midstorey thickets. As thickets grew upward, Q. rubra regeneration became more stratified and in some instances, produced a dense sub-canopy which appeared to greatly reduce light penetration to the forest floor. This likely contributed to the negative relationship observed between seedling height and Shannon diversity. Variables measured in this study explained 40% of the observed variation in seedling height and 25% of the variation in seedling diameter, suggesting other influential factors that were not quantified in this study. Given the findings of Vor (2005), we believe that some of the remaining variation can be attributed to deer browsing. In North America, successful regeneration of Q. rubra requires an adequate reservoir of advanced regeneration at the time of harvest (Carvell and Tryon, 1961; Steiner et al., 1993) and the creation and maintenance of an appropriate light environment (Phares, 1971; Loftis, 1990). Current shelterwood techniques attempt to

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provide a favourable light environment through partial harvests aimed at reducing basal area to some ideal level; often thought to be 60–70% of that of the unharvested forest (Loftis, 1992). While emphasis is frequently placed on sub-canopy removal, such harvests often result in a substantial reduction in canopy closure producing a heterogeneous light environment at the forest floor which can allow the proliferation of undesirable plant species (Dech et al., 2008; Parker and Dey, 2008). Our findings indicate that Q. rubra seedling establishment may respond more to the degree of stand stratification (e.g. midstorey density) than canopy closure itself. Once midstorey competition has been completely removed, the relatively uniform shade cast by closed canopies may be acceptable or even beneficial to Q. rubra seedlings provided that light levels remain above 30% full sunlight (Phares, 1971). North American prescriptions could benefit from midstorey tending and only minor overstorey thinning in years prior to shelterwood harvests to permit the development of adequate seedling stocks. Whenever possible, this should be performed immediately following mast years. The retention of an adequate number of seed trees upon partial harvest is also critical. Similar recommendations have recently been proposed by Stringer (2006) but are not yet commonly practiced in North America. Managers of North American forests invest substantial effort and expense in their attempts to promote the regeneration of native Q. rubra populations through series of partial harvests, tending, vegetation control, prescribed fire, etc., yet such efforts do not result in an abundance of regeneration remotely equivalent to the unassisted regeneration observed in Freiburg and elsewhere in Europe where natural regeneration of Q. rubra is often successful in the absence of silvicultural promotion. Our study illustrates that despite poor regeneration in its native range, Q. rubra has the ability to perform as an effective competitor when conditions permit. The regeneration failure of Q. rubra in North America is strongly linked to a decreased disturbance frequency due to fire suppression and the inability of this mid-tolerant species to compete in sub-canopy strata with shade-tolerant tree species under closed canopies. In Europe, where fire disturbances are rare, we observed that under relatively closed canopies and in the presence of shadetolerant tree species, the regeneration of Q. rubra required no silvicultural intervention to be consistently successful. Shade does not appear to limit the regeneration of Q. rubra in Europe as it does in North America. Future research seeking to explain the success of this species in Europe should confirm whether: (1) Q. rubra exhibits greater shade tolerance; (2) ‘‘closed’’ forest canopies permit greater light transmission; and (3) competition from shade-tolerant tree species is less severe, in the forests of Europe where Q. rubra is important compared to those in North America.

Acknowledgments We are grateful to Peter Ryser, Winfried Meier, Patrick Pyttel Carl Höcke and Ernst Kraemer for their insights into various aspects of this study; Marie-Cécile Gruselle, Anja Hausmann and Ursula Eggert for logistic support in Freiburg; and Kevin Pigeau and Margaret McGrath for assistance in the field. This study was funded by the Ontario Centres of Excellence, Natural Sciences and Engineering Research Council of Canada and Ontario/BadenWürttemberg Student Exchange Program.

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