Belowground facilitation and competition in young tree species mixtures

Forest Ecology and Management 265 (2012) 191–200

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Belowground facilitation and competition in young tree species mixtures Pifeng Lei a,b,⇑, Michael Scherer-Lorenzen c, Jürgen Bauhus a a

Institute of Silviculture, Faculty of Forest and Environmental Sciences, University of Freiburg, Germany Faculty of Life Science and Technology, Central South University of Forestry and Technology, China c Faculty of Biology, Geobotany, University of Freiburg, Germany b

a r t i c l e

i n f o

Article history: Received 24 August 2011 Received in revised form 23 October 2011 Accepted 26 October 2011 Available online 24 November 2011 Keywords: Fine root morphology Tree species richness Niche complementarity Morphological plasticity Size-asymmetric competition

a b s t r a c t Belowground interactions in diverse plant communities may be decisive for the performance of individual species and community stability. Here we assessed the effect of tree species richness on belowground fine-root morphology and belowground competition between four different species in a 6-year-old field biodiversity experiment to test the hypotheses: (i) overall fine-root exploitation (total fine-root length and surface area) increases with tree species richness; (ii) belowground interspecific competition is size-symmetric. Overall fine-root length and surface area in the centre of neighbourhoods of four saplings were initially low (1.03 km m2 and 2.00 m2 m2), but reached 3.13 km m2 and 6.50 m2 m2, respectively, across all species combinations after two growing seasons in the ingrowth cores. However, no significant differences were found among the different tree species richness levels. The saplings of different tree species grew in proportion to their initial sizes with respect to aboveground basal area increments. For belowground fine-root growth in mixed neighbourhoods, however, Pseudotsuga menziesii and Picea abies had higher fine-root growth rates in ingrowth cores than in monocultures, whereas the reverse was true for Fagus sylvatica and Quercus petraea. After two years of root ingrowth, the competitive ability indexes (P. abies = 0.07, P. menziesii = 0.08, F. sylvatica = 0.19, Q. petraea = 0.18) revealed that belowground competition in this sapling stand was size-asymmetric and that conifers showed a higher competitive ability, when fine-root growth was related to aboveground standing basal area. Nutrient enrichment in ingrowth cores did not affect proliferation rates and morphology of fine roots significantly. Fine-root morphologies of different species were remarkably different, but within each species the morphology was not significantly influenced by tree species richness of neighbourhoods. Our results show that belowground competition may occur earlier than aboveground in mixed forest stands and fine-root growth of dominant species benefitted more from mixing with other species than that of inferior species. Ó 2011 Elsevier B.V. All rights reserved.

1. Introduction Accumulating evidence of positive effects of biodiversity on ecosystem functioning, such as productivity, stability and nutrient retention, from grassland ecosystems has resulted in a number of studies conducted experimentally or observationally to test whether these patterns also occur in forest ecosystems (SchererLorenzen et al., 2007; Potvin and Gotelli, 2008; Meinen et al., 2009b; Potvin and Dutilleul, 2009; Bruelheide et al., 2011). Two recent studies examining the effects of tree species diversity on belowground productivity showed that fine-root production in polycultures was higher in species-rich stands than in species-poor ⇑ Corresponding author. Address: Institute of Silviculture, University of Freiburg, Tennenbacherstr. 4, 79106 Freiburg i. Br., Germany. Tel.: +49 761 203 86 21; fax: +49 761 203 37 81. E-mail address: [email protected] (P. Lei). 0378-1127/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2011.10.033

stands or monocultures (Meinen et al., 2009b; Brassard et al., 2011), although standing root biomass remained unchanged in one study (Meinen et al., 2009a). Regarding soil exploitation and belowground resource capture, however, fine-root morphological traits (e.g. length and surface area), analogue to leaf area for photosynthesis, and the spatial distribution of fine roots may be more relevant for species interactions than fine-root dry mass (Bolte and Villanueva, 2006). To our knowledge, there have been only few studies taking fine-root morphology into account. In these studies, there were either no effects (Hendriks and Bianchi, 1995; Bauhus et al., 2000) or negative effects (Bolte and Villanueva, 2006) of species admixing on the fine-root length density in two-species mixtures compared to corresponding monocultures. It is surprising since positive diversity-productivity relationships have been found in most cases in artificial grasslands (Hector et al., 1999; Cardinale et al., 2007; Mommer et al., 2010) and also in many mixed forest stands (Bauhus and Schmerbeck, 2010). Below ground, however,

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this positive relationship between diversity and productivity has not been tested with regard to fine-root length and soil volume occupation in artificial and diverse forest communities yet. Co-existing species in the same stand compete with each other for soil nutrients and water, which is a main force underlying the structure and dynamics of plant communities. In contrast to aboveground interactions, where larger plants have disproportional advantages for light and therefore competition is usually asymmetric, belowground competition is more likely to be symmetric, i.e. the individual plants compete for soil resources in proportion to their size (Casper and Jackson, 1997; Cahill, 2003). Belowground symmetric competition is mainly attributable to the equal chances of encountering, accessing and using soil resources by roots of different species, which has been found in herbaceous communities growing in homogeneous soil (Casper and Jackson, 1997; Cahill and Casper, 2000; Schenk, 2006). However, in herbaceous communities growing under conditions of heterogeneous nutrient supply and in mixtures of woody species, asymmetric belowground competition has been observed (Rajaniemi, 2003; Rewald and Leuschner, 2009a,b). In addition, nutrient availability may act as a potential source of variability in biodiversity experiments and alter the competitive interactions between different species (Fransen et al., 2001; Fridley, 2001). All plants, despite their immobility, are capable to adapt to different abiotic conditions (e.g. nutrients) and biotic conditions (e.g. neighbouring species) through changing the belowground rooting strategy and foraging ability (Fransen et al., 1998; Pergitzer et al., 2002; Messier et al., 2009). Plants may adopt either extensification strategies by increasing investment of carbon into fine roots or intensification strategies by altering absorption efficiency through morphological plasticity, or both (Ostonen et al., 2007a; Bonifas and Lindquist, 2009). Morphological plasticity is one of the most important responses to environmental changes (Fitter, 1987; Lohmus et al., 1989). For example, specific root length (SRL) has been suggested as an indicator of nutrient availability for a series of European tree species under experimental conditions (Ostonen et al., 2007b). Morphological adjustment will change the fine-root cost/benefit ratio, thus change the fine root soil-exploitation efficiency per unit carbon invested in the entire fine-root system or the individual rootlet (Leuschner et al., 2009). Analyses of fine-root branching order systems revealed that the root tips (or first-order roots) are the most important sections of fine-root systems for nutrient and water acquisition, and that these are also very sensitive to environmental changes (Pergitzer et al., 2002; Guo et al., 2004; Wang et al., 2006; Hishi, 2007). Compared to mature forests, fine-root adaptation strategies may be more pronounced and significant for young trees, because large trees have a greater ability to control the internal nutrient and carbohydrate mobilisation (Leuschner et al., 2004). Furthermore, belowground interactions between tree species may be more pronounced in young tree communities, when the fine-root systems of different species first encounter each other and have not yet developed patterns to avoid hetero-specific neighbours, for example through vertical stratification. Here we present results from a 6-year-old tree species diversity experiment, where the number of tree species was experimentally controlled in the form of a replacement series design. In this study we aimed to test the hypotheses that (i) overall fine-root exploitation (total fine root length and surface area) increases with neighbourhood tree species richness; (ii) fine root morphology changes with tree species richness; (iii) belowground interspecific competition is size-symmetric, and (iv) root proliferation in nutrient-enriched soil patches is higher in diverse neighbourhoods than monocultures.

2. Materials and methods 2.1. Study site and sample collection The experimental site was located near Kaltenborn in Thuringia, Germany (10°130 E, 50°470 N). It is part of the BIOTREE experiment, a 6-year-old biodiversity-ecosystem functioning experiment with temperate tree species. The site is situated in the Southern Thuringian Trias between the mountain regions of Thuringian Forest and Rhön with acidic sandstone bedrock, which developed to arenosols with low cation exchange capacity. The climate is Sub-Atlantic with a mean annual temperature of 7.8 °C and mean annual precipitation of 650 mm. In all horizons sand content was >75% with a loamy sand texture. The soil is acidic (pHKCl, 4.5–5.0) with low cation exchange capacity (3.6–5.8 cmolc kg1), and total N concentrations ranging from 0.02% to 0.19% in top 30 cm of the soil profile (Scherer-Lorenzen et al., 2007). Until 1975, the site was used as cropland and then converted to grassland, where the ground vegetation was dominated by Holcus lanatus L. and Bromus hordeaceus L. Before afforestation, the planting rows were prepared with a deep-spade moulding cutter for 30 cm width and 60 cm depth. Seedlings of four tree species, including two deciduous species, European beech (Fagus sylvatica L.) and Sessile oak (Quercus petraea Liebl.), and two conifers, Norway spruce (Picea abies (L.) Karst.) and Douglas fir (Pseudotsuga menziesii), were planted in a grid with two planting densities (1 m  1.5 m and 2 m  1.5 m) in 36 plots of 16 m  16 m in winter 2003/2004. Three planting protocols, centroides (equal proportion of each species, i.e. 25:25:25:25), corner points (one dominated species with high proportion, i.e. 70:10:10:10), or midpoints (one subordinated species with lower proportion, i.e. 10:30:30:30) were applied and replicated in two blocks following a simplex design. The positions of plots within blocks, and the positions of each tree species within plots were placed at random. This study was carried out only in the 18 plots with high planting density (1 m  1.5 m), equivalent to a stem density of 6667 ha1. More details about the study site and the plantation layout are provided elsewhere (Don, 2007; SchererLorenzen et al., 2007; Lei and Bauhus, 2010). In a first step, fine-root samples were extracted from undisturbed soil in March 2008. Four soil cores of 4.7 cm in diameter and 30 cm in depth were taken from the centre of the rectangle cornered by four saplings (Fig. 1). A preliminary survey had shown that very few fine roots occurred below 30 cm soil depth. These squares, thereafter called neighbourhoods, were selected randomly from 18 plots in accordance with a series of species combinations, ranging from one-, two-, three- and four-species mixtures, including four monoculture combinations, six two-species mixture combinations, four three-species mixture combinations with two conifers and two deciduous saplings and one four-species mixture with six replicates (Fig. 1, Table 1). The four soil cores from one neighbourhood were combined and split into two layers (0–15 cm and 15–30 cm), to investigate whether species interactions and tree diversity effects were influenced by soil depth. Equal distances from the sampling location to the corners of the rectangular neighbourhoods ensured equal potential influence of each tree/species in the neighbourhood. To measure fine-root growth, ingrowth cores with 3 mm nylon mesh were installed, in a second step, at the location of the holes created by soil cores (6.5 cm in outer diameter). They were filled with sieved, root free soil (4.5 mm mesh) taken from the vicinity of the experimental plots. Half of them were assigned to a ‘‘high nutrient patch treatment’’, where the soil for each core was mixed with 4.5 g of fertilizer (equivalent to 1080 kg N ha1, 810 kg P2O5 ha1, 1490 kg K2O ha1, 405 kg MgO ha1) before refilling. The other half of the cores remained untreated. These nutrient enrichment rates are high

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1 species

2 species

X

0.5 m

0.5 m

0.5 m

3 species

X

Y

X

X

X

X

Y

Y

X

X

Z

Y

0.33 m 0.34 m 0.33 m

X

4 species

Z

W

Fig. 1. Experimental design and sampling position for fine-root collection at the transition zone of four saplings from Kaltenborn, one of three BIOTREE sites. W, X, Y and Z represent the different species of F. sylvatica, Q. petraea, P. abies and P. menziesii. Four soil cores or ingrowth-cores were combined as one sample and sliced to two layers (0– 15 cm and 15–30 cm).

Table 1 Layout of sampling combination neighbourhoods and number of fine root sampling replicates. Species symbols are F. sylvatica (b), Q. petraea (o), P. abies (s) and P. menziesii (d). Species richness

1

Combinations

bbbb

oooo

ssss

dddd

2 bboo

bbss

bbdd

ooss

oodd

ssdd

boss

bodd

bbsd

oosd

bosd

Soil cores March 2008 Fertilised ingrowth cores harvested in October 2008 Unfertilised ingrowth cores harvested in October 2008 Fertilised ingrowth cores harvested in October 2009 Unfertilised ingrowth cores harvested in October 2009

6 3

6 3

6 3

6 3

6 3

6 3

6 3

6 3

6 3

6 3

6 3

6 3

6 3

6 3

6 4

3

3

3

3

3

3

3

3

3

3

3

3

3

3

4

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

6

compared to conventional rates for surface applications. However, we wanted to create nutrient-rich patches throughout the installed 30 cm soil depth. This would not have been achievable with smaller quantities, which could also not have been effectively mixed with the quantity of soil used for ingrowth cores. To avoid confounding effects and interference from roots of grasses, which were completely covering the ground at the beginning of the ingrowth experiment, the herbicide glyphosate was sprayed at a concentration recommended for grass covers (5 L ha1) in the central area of the tree neighbourhoods following the installation of ingrowth cores. Previous studies showed that glyphosate had little or no effect on soil microbial communities at typical field rate applications (Busse et al., 2001). We assumed it would not affect the growth of fine roots. The ingrowth cores were harvested after one and two growing seasons (October 2008 and October 2009). For analysis, four ingrowth cores from the centre of each sampling square were combined to form one sample for each layer (0–15 cm and 15–30 cm), similar to the samples from undisturbed soil. The species combinations and sampling replicates are listed in Table 1. To relate belowground interactions to those above ground, all the saplings surrounding the fine-root sampling neighbourhoods were recorded. We measured all the 1088 saplings surrounding 272 neighbourhoods, resulting in 272 saplings for each species. The diameter at 10 cm height above ground level (D10) was measured using calipers, sapling height with a height pole and ruler in June 2008 and October 2009 (Table 2). The leaf area index

3

4

(LAI) was estimated with a method similar to that used by Gower and Norman (1991). Ten trees of each species were selected according to the measured D10 frequency distribution. The live crown was divided to three sections with equal length. At each sections (upper, middle and lower), diameter of all the branches were recorded with calipers and one branch with average diameter from each section was removed for leaf area measurement. The projected leaf area was measured with a leaf-area meter (Li-COR3100, Li-COR, Lincoln, Nebraska) for the deciduous species. The one-sided needle area of coniferous species was scanned and analysed with WinRhizo 2005 (Regents Instruments, Quebec, Canada). Allometric equations to predict leaf area of individual saplings for each species were based on the following function:

logY ¼ a þ b logðD10 Þ where Y is projected leaf area (m2) and D10 is stem diameter (cm) at 10 cm height above the ground level (Table 3). For the sake of simplicity and efficiency, we developed allometric equations to predict leaf area based on stem diameters rather than the often used sapwood area (Jonckheere et al., 2004; Calvo-Alvarado et al., 2008). It has been shown in previous studies that this type of equation can provide accurate estimates of projected leaf area (Gower and Norman, 1991). Furthermore, the young saplings at our study site would not have formed much heartwood yet, hence most cross-sectional area of stems would have comprised sapwood.

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Table 2 Aboveground characteristics of F. sylvatica, Q. petraea, P. abies and P. menziesii saplings in June 2008 and October 2009 (n = 272 saplings for each species). Basal area (m2 ha1)

Leaf area Index (m2 m2)

Sapling height (m)

Mean D10 (cm)

June 2008 F. sylvatica Q. petraea P. abies P. menziesii

1.91 ± 0.41 1.60 ± 0.47 2.13 ± 0.41 3.07 ± 0.57

a b c d

2.46 ± 0.57 2.19 ± 0.66 4.32 ± 0.78 5.71 ± 1.23

a b c d

0.83 ± 0.39 0.68 ± 0.41 2.52 ± 0.85 4.47 ± 1.80

a a b c

1.41 ± 0.65 1.83 ± 0.88 2.26 ± 0.71 2.02 ± 0.57

a b c d

October 2009 F. sylvatica Q. petraea P. abies P. menziesii

2.90 ± 0.61 2.51 ± 0.73 3.33 ± 0.70 4.86 ± 0.77

a b c d

3.83 ± 0.88 3.45 ± 1.13 6.78 ± 1.33 8.92 ± 1.85

a b c d

2.02 ± 0.88 1.72 ± 1.11 6.25 ± 2.37 10.87 ± 4.35

a a b c

2.30 ± 0.89 2.06 ± 1.39 3.54 ± 1.14 3.33 ± 1.05

a b c c

Given are means ± SD. Different letters indicated significant difference between different species at P < 0.05.

Table 3 Allometric equations between projected leaf area (m2) and stem diameter (cm) at 10 cm height above ground level for F. sylvatica, Q. petraea, P. abies and P. menziesii. Y indicates the projected leaf area; D10 indicates the stem diameter at 10 cm height above ground level. Species

Allometric equation

R2

F. sylvatica Q. petraea P. abies P. menziesii

log log log log

0.943 0.912 0.833 0.907

Y = 1.6219 + 2.1736 log (D10) Y = 0.9736 + 1.5111 log (D10) Y = 1.4988 + 1.8524 log (D10) Y = 1.69 + 1.9862 log (D10)

2.2. Processing of root samples Fine roots were cleared off the soil using the floatation method above a 1.0 mm mesh sieve under regular tap water (Böhm, 1979; Bauhus and Bartsch, 1996). Tree roots longer than 1.0 cm were separated from the grasses and herbs roots, which were generally white to light yellow, finer and less ramified than tree roots. The tree roots were further sorted visually into live and dead fractions by species according to morphological characteristics with reference samples (Bauhus and Messier, 1999; Leuschner et al., 2001). Here the size and colour of the most distal root section, branching pattern (angle and ramification density) and periderm surface structure were used for species identification. The dead fine roots were brittle and easily fractured and were characterised by a dark to grey cortex and stele. In this study, only live tree fine roots (62.0 mm in diameter) were analysed. The sorted fine-root samples of each species were dispersed in water in a transparent tray and scanned with 400 dpi resolution. The images were analysed with low smoothing filter for coarse coniferous species roots and without smoothing filter for thin deciduous species roots using the software WinRhizo™ 2009 (Regent Instruments, Quebec, Canada). After measurements, roots were oven dried to constant weight at 40 °C. Specific root length (SRL) (m g1) and specific root area (SRA) (m2 g1) were calculated with total length and total surface area divided by the root dry mass of the corresponding sample, respectively. To measure fine root morphology, we selected one or two largely intact, highly ramified fine-root sections from each sample, in cases where intact ones were available. The surface area and diameter of fine root tips were analysed using the link analysis tool provided by WinRhizo™ 2009. Since the external–external links and external–internal links are not physiologically different, they were grouped as root tips. Root fragments can account for a substantial proportion of the total fine-root biomass and length (Bauhus and Bartsch, 1996). To quantify the length and surface area of broken rootlets shorter than 1.0 cm left over following the sorting process, an extrapolation method based on biomass and SRL or SRA was applied in two steps. Firstly, the dry weight of remaining root fragments

was estimated using a sampling approach by collecting 10% of the area of a tray on which root residues were evenly distributed in water. This method proved to be very efficient (Bauhus and Bartsch, 1996). The collected root fragments were dried for at least 72 h at 40 °C to constant weight and weighed to 0.0001 g. The mass of short root fragments of each sample was multiplied by 10 and this value was distributed proportionally according to the fractions sorted by species, and dead and live status for the entire root sample. Secondly, the length and surface area of root fragments of each species was calculated through multiplication of the proportional biomass of each species determined in step one with the particular specific root length (SRL) or specific root area (SRA) for corresponding species measured from that particular root sample longer than 1.0 cm. However, this indirect method is likely to underestimate the true length and surface area of the short fragments, because SRL or SRA of residuals is based on larger fine-root sections that are probably thicker on average. 2.3. Data analysis All calculations and statistical analyses were conducted with R (R2.11.1) (R Development Core Team, 2010). Effects of nutrient enrichment on overall fine-root morphology (total length and surface area) and architectural traits were tested with t-test or Mann– Whitney U test (Wilcoxon’s rank test) between samples from nutrient-enriched ingrowth cores and untreated ingrowth cores. Overall fine-root length and total surface area did not differ significantly between nutrient-enriched soil patches and unfertilised soil in ingrowth cores. The same was true for fine-root length, surface area, or morphological characteristics of individual species. Therefore, the data from nutrient-enriched and no fertilizer treated ingrowth cores were pooled for further analysis. To quantify the competitive ability of a given species in mixed neighbourhoods, the competitive ability index (CA), suggested by Rewald and Leuschner (2009a), was applied to assess the fitness of target species competing with neighbouring species. However, in our experiment with a replacement series design, it would have been inappropriate to compare intraspecific interaction with interspecific interactions with the absolute fine-root elongation or production values directly (Goldberg, 1996), since the abundance of a given tree species in mono-specific neighbourhoods was always higher than in hetero-specific neighbourhoods (four saplings versus two or one sapling for a given tree species). Therefore, we calculated the CA of a given species in mixed neighbourhoods based on adjusted fine-root length produced in ingrowth cores per unit standing basal area (FRL) (m m2 m2 BA) in mixed and mono-specific neighbourhoods (Bolte and Villanueva, 2006) using the following equation:

CA ¼ ðFRLmix  FRLmono Þ=FRLmono

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undisturbed soil, nor for the fine roots that had grown in the ingrowth cores after one and two growing seasons (Fig. 2). The total length and surface area of live tree fine roots derived from standing natural soil was low at the beginning of the ingrowth experiment with an average of 1.03 km m2 and 2.00 m2 m2, respectively. Fine-root length in ingrowth cores after one and two growing seasons was on average 1.25 times and 3 times higher than the initial standing fine-root length, respectively. There were no significant differences detected for fine-root length density and surface area between nutrient-enriched and untreated ingrowth cores (P > 0.05) after one and two growing seasons. After two growing seasons, root length density was on average 3.19 km m2 in unfertilised ingrowth cores and slightly higher than that in nutrientenriched ingrowth cores (3.06 km m2). Among the live fine roots produced in ingrowth cores after one and two growing seasons, P. abies contributed the highest proportion (40.8%) followed by P. menziesii, which accounted for 36.3% of live fine-root mass, although P. menziesii represented 52.6% of aboveground basal area. In contrast, F. sylvatica produced 16.4% and Q. petraea 6.6% of fine-root biomass in ingrowth cores (Fig. 3).

Positive CA values indicate greater fine-root growth rate for a given species in mixtures than in monocultures. Similar values of the different species in mixture denote symmetric competition. Likewise, high differences in CA values between participating species can be interpreted as asymmetric competition between the species in mixture (Rewald and Leuschner, 2009a). 3. Results 3.1. Aboveground structure In this young afforested stand, the conifers were apparently the dominant species with respect of aboveground growth (Table 2). In the initial and final stages of this study, the contribution of each species to the total basal area were quite similar, where P. menziesii accounted for 52.7% and 52.3% and P. abies comprised 29.5% and 29.9% of basal area at the beginning and end of the this experiment, respectively. Among the deciduous species, F. sylvatica contributed 9.8% and 9.7%, and Q. petraea 8.0% and 8.2% to the total basal area in June 2008 and October 2009, respectively. Leaf area index (LAI) was significantly different among the different species at both sampling occasions and increased over time (Table 2).

3.3. Competitive ability index in mixed-species neighbourhoods

3.2. Belowground fine-root growth

Striking differences between different species were observed for the competitive ability index (CA), which was calculated based on the fine-root length produced in ingrowth cores per unit standing basal area for each companion species. After one growing season,

Overall fine-root length and surface area was neither significantly different among different species richness levels in

A

B

2.0

2

C

4

1.2 1.5

3

1.0

2

0.5

1

1.0 0.8

0-15 cm

0.6 0.4 0.2

15-30 cm

0.0

0.0

3.0

5

0

−2

Live fine root surface area (m m )

−2

Live fine root length (km m )

1.4

8 2.5

4

2.0

6 3

1.5

0-15 cm

4

2 1.0

2

1

0.5

15-30 cm

0.0

0

1

2

3

4

1

2

3

4

0

1

2

3

4

Species richness Fig. 2. Total live fine-root length and surface area at different species richness levels in undisturbed soil (A), ingrowth cores after one growing season (B) and ingrowth cores after two growing seasons (C). Bars represent means ± SE. Differences between species richness levels were non-significant (P > 0.05).

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Basal area P.abies

Live fine root mass Q.petraea Q.petraea F.sylvatica

P.abies

F.sylvatica

P.menziesii

P.menziesii

Fig. 3. Relative proportion of F. sylvatica, Q. petraea, P. abies and P. menziesii in aboveground basal area and live fine-root mass in ingrowth cores.

coniferous species showed much higher fine-root length per unit basal area in the mixed neighbourhoods than in mono-specific neighbourhoods. Fine-root length per unit basal area of P. menziesii and P. abies increased by 162% and 41%, respectively, over the first growing season. This occurred at the expense of the deciduous species, for which root length per unit basal area declined by 56% and 10% for F. sylvatica and Q. petraea, respectively (Table 4). During the second growing season, CA values returned to a small range around 0, where CA values ranged from minus 0.19 for F. sylvatica to 0.08 for P. menziesii. However, the differences between the coniferous and deciduous species were still significant (P < 0.05). Furthermore, the response of a given species to the presence of another species in mixed neighbourhoods changed with neighbouring species identity. For example, P. menziesii showed significant differences among different mixed neighbourhoods at both sampling occasions. Also, fine roots of F. sylvatica grew better in beech-spruce mixed neighbourhoods compared to the other mixtures in the first growing season, although the CA for F. sylvatica was still negative. Comparing the CA values of different companion species in particular mixedspecies combinations it showed that co-occurring species

responded in most cases differently to admixing, where the CA was positive for one companion species and negative for another. These contrasting responses between different companion species were much more obvious in the mixed neighbourhoods containing coniferous and deciduous species. For example, the CA values were positive for conifers and negative for hardwoods during the first growing season, indicating P. menziesii and P. abies produced more fine roots, while F. sylvatica and Q. petraea produced fewer fine roots in the mixed stands than in monocultures. The high belowground competitive strength of the two coniferous species and low competitiveness of the two deciduous species were also reflected by their RAI/LAI ratios, which were higher for conifers in hetero-specific than in mono-specific neighbourhoods, and were lower for hardwoods at both sampling occasions (Table 5). Although significant differences between mono-specific and hetero-specific neighbourhoods were only detected for F. sylvatica after the first growing season, this was mainly due to the high within-species variation. For example, the ratio of RAI/LAI for P. menziesii in mixed neighbourhoods was over two times higher than that in monocultures, but the difference was statistically not significant.

Table 4 Competitive ability index (CA) of F. sylvatica, Q. petraea, P. abies and P. menziesii for belowground interspecific interactions with different neighbouring species based on fine-root length produced in ingrowth cores per unit of basal area. Given are means ± SE. Different small letters indicate significant differences among different mixture combinations, P < 0.05. Different capitals indicate significant differences among different species, P < 0.05. Combinationsa

a

F. sylvatica

Q. petraea

P. abies

Ingrowth cores harvested after one growing season bboo 0.69 ± 0.11 b bbss 0.24 ± 0.17 a bbdd 0.75 ± 0.07 b ooss – oodd – ssdd – boss 0.55 ± 0.14 ab bodd 0.81 ± 0.10 b bbsd 0.55 ± 0.14 ab oosd – bosd 0.42 ± 0.35 ab Mean 0.56 ± 0.08 A

0.72 ± 0.71 – – 0.06 ± 0.48 0.59 ± 0.88 – 0.64 ± 0.17 0.08 ± 0.42 – 0.40 ± 0.28 0.62 ± 0.14 0.10 ± 0.19

a

Ingrowth cores harvested after two growing seasons bboo 0.16 ± 0.23 a bbss 0.20 ± 0.13 a bbdd 0.20 ± 0.16 a ooss – oodd – ssdd – boss 0.23 ± 0.29 a bodd 0.39 ± 0.16 a bbsd 0.44 ± 0.06 a oosd – bosd 0.01 ± 0.24 a Mean 0.19 ± 0.07 A

0.10 ± 0.29 – – 0.07 ± 0.25 0.15 ± 0.20 – 0.11 ± 0.35 0.45 ± 0.15 – 0.27 ± 0.15 0.29 ± 0.17 0.18 ± 0.09

a

Species symbols are F. sylvatica (b), Q. petraea (o), P. abies (s) and P. menziesii (d).

a a a a a a A

a a a a a a A

– 0.24 ± 0.16 – 0.17 ± 0.43 – 0.09 ± 0.25 0.31 ± 0.17 – 0.88 ± 0.70 0.40 ± 0.61 1.15 ± 0.58 0.41 ± 0.18 – 0.06 ± 0.11 – 0.10 ± 0.11 – 0.15 ± 0.17 0.13 ± 0.16 – 0.27 ± 0.13 0.24 ± 0.16 0.67 ± 0.42 0.07 ± 0.08

P. menziesii

a a a a a a a B

a a a a a a a B

– – 2.60 ± 1.46 – 2.49 ± 1.11 0.72 ± 0.74 – 3.39 ± 0.78 0.11 ± 0.18 2.17 ± 1.45 0.28 ± 0.43 1.62 ± 0.38 – – 0.17 ± 0.12 – 0.43 ± 0.20 0.12 ± 0.19 – 0.59 ± 0.21 0.18 ± 0.17 0.16 ± 0.20 0.16 ± 0.27 0.08 ± 0.08

ab ab ab a b ab b C

b a bc a bc bc c B

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P. Lei et al. / Forest Ecology and Management 265 (2012) 191–200 Table 5 The ratio of fine-root area index to leaf area index (RAI/LAI) of F. sylvatica, Q. petraea, P. abies and P. menziesii in mono-specific and mixed neighbourhoods. Asterisks denote significant differences between mono-specific and mixed neighbourhoods with Mann–Whitney U test, P < 0.05. Data show means ± SE. P. abies

P. menziesii

Ingrowth cores harvested after one growing season Monocultures (n = 6) 1.65 ± 0.35⁄ 0.91 ± 0.30 Mixtures (n = 44) 0.89 ± 0.17⁄ 0.96 ± 0.19

F. sylvatica

Q. petraea

0.64 ± 0.11 0.97 ± 0.13

0.12 ± 0.04 0.25 ± 0.04

Ingrowth cores harvested after two growing seasons Monocultures (n = 12) 2.71 ± 0.32 1.33 ± 0.25 Mixtures (n = 84) 2.29 ± 0.22 1.01 ± 0.10

1.81 ± 0.14 1.93 ± 0.15

0.69 ± 0.14 0.82 ± 0.06

3.4. Fine root architectural characteristics and plasticity Fine-root morphological parameters were significantly different between fine roots of deciduous and coniferous saplings. Fine roots of P. menziesii and P. abies were significantly thicker and showed significantly lower SRL than those of F. sylvatica and Q. petraea (Table 6). The average fine-root diameter increased in the order F. sylvatica, Q. petraea, P. abies and P. menziesii, with significant differences among them. This was also true for the surface area and diameter of fine-root tips. When comparing the fine-root morphological characteristics in different soil layers, fine roots including their tips were usually thicker in the deeper layer (15–30 cm) than those in the surface soil layer for all the species (0–15 cm) (Table 6). Correspondingly, fine roots in topsoil tended to have a higher SRL than in the lower soil layer, although only P. abies showed significant differences between different soil layers in the undisturbed soil in terms of fine-root diameter. The overall fine-root SRL and mean diameter varied remarkably in the neighbourhoods with increasing tree species richness, but neither SRL nor mean diameter of the entire fine-root system showed significant differences among different species richness levels for all tree species here. There were some significant differences within species detected from analyses of intact fine-root sections among different tree species diversity levels, although most of them seemed to fluctuate substantially (Fig. 4). Notably, the surface area and diameter of F. sylvatica fine-root tips increased, whereas the mean diameter of P. menziesii root tips declined consistently with increasing species richness. 4. Discussion 4.1. Belowground fine-root interactions After 5 years of growth, total tree fine-root length and surface area in the undisturbed soil were quite low in this experiment. However, fine-root length density in the ingrowth cores after two

growing seasons was similar to values reported previously for mature beech-spruce stands (Bolte and Villanueva, 2006) and beechDouglas fir stands (Hendriks and Bianchi, 1995). The high fine-root length density in ingrowth cores might be attributed to the high planting density in this young afforested stand (1 m  1.5 m), high fine-root expansion rate of the saplings (Table 2), and the herbicide application. The dense herb and grass layer at the beginning of the ingrowth experiment might have suppressed tree fine-root growth in the undisturbed soil initially. Therefore, to quantify the interspecific competition between different tree species, we mainly compared fine-root growth in the ingrowth cores. The main purpose of this study was to investigate whether the soil exploitation ability of fine roots in diverse communities was higher than in less diverse and single species communities. Higher productivity of fine roots in species-rich stands compared to species-poor or mono-specific stands were reported previously (Meinen et al., 2009b; Brassard et al., 2011). This kind of belowground over-yielding may result from niche differentiation due to different spatial rooting patterns of participating species, thus leading to lower interspecific competition compared to intraspecific competition. Our results, in contrast, showed that total fine-root length or surface area did not differ significantly among different tree species richness levels, neither in the undisturbed soil, nor in the ingrowth cores. Previous studies comparing fineroot length density in two species mixtures with monocultures also showed similar results (Hendriks and Bianchi, 1995; Bauhus et al., 2000), and even lower fine-root length density in mixed stands when compared to monocultures was reported (Bolte and Villanueva, 2006). These contradictory results make fine-root interactions complicated to monitor and interpret, mainly owing to the differences of soil exploitation efficiency and capacity of fine roots at different locations, sites, climate and species involved (Kalliokoski et al., 2010). Interspecific competition or interference of neighbouring species is usually assessed by the reduction in growth and survivorship of the target species. In this sapling stand, the conifers grew faster than the hardwoods, but the basal area increments of each species were in proportion to their initial sizes, as the contributions of each species to the total basal area at the end of this study were similar to the corresponding proportion of the given species at the beginning. The aboveground size-symmetric basal area increments may indicate that aboveground competition for light is not yet limiting in this sapling stand (Weiner and Thomas, 1986). Meanwhile, the time intervals used to assess aboveground growth may have been simply too short to identify any species differences. Compared to their relative contributions to basal area, P. abies and F. sylvatica produced proportionately more fine-root length in the ingrowth cores, e.g. P. abies produced 40.8% of fine-root biomass while contributing to 29.5% of basal area only. The

Table 6 Specific root length (SRL), mean diameter of the fine-root system, and diameter and surface area of root tips of F. sylvatica, Q. petraea, P. abies, and P. menziesii at 0–15 and 15–30 cm soil depth in undisturbed soil (n ranges from 31 to 47 samples for each species).

Fine root system SRL (m g1) Diamter (mm) Fine root tips Diameter (mm) 2

Surface area (mm )

Depth

F. sylvatica

Q. petraea

P. abies

P. menziesii

0–15 15–30 0–15 15–30

33.52 ± 2.74 a 29.64 ± 3.10 a 0.377 ± 0.024 a 0.388 ± 0.017 a

41.32 ± 6.74 a 36.22 ± 5.14 a 0.402 ± 0.026 a 0.438 ± 0.021 a

11.12 ± 0.72 b 9.28 ± 0.51 b 0.639 ± 0.011 b⁄ 0.766 ± 0.025 b⁄

7.40 ± 0.50 c 7.87 ± 0.58 c 0.858 ± 0.022 c 0.917 ± 0.029 c

0–15 15–30 0–15 15–30

0.116 ± 0.001 0.112 ± 0.002 0.392 ± 0.014 0.380 ± 0.016

0.129 ± 0.002 0.120 ± 0.003 0.498 ± 0.023 0.442 ± 0.031

0.249 ± 0.003 0.288 ± 0.005 1.436 ± 0.046 1.911 ± 0.161

0.403 ± 0.008 0.411 ± 0.011 3.892 ± 0.228 4.018 ± 0.329

a⁄ a⁄ a a

b⁄ b⁄ b a

c⁄ c⁄ c⁄ b⁄

d d d c

Data show means ± SE. Different letters indicate significant differences between different species and asterisks indicate significant differences between different soil layers at P < 0.05.

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Fig. 4. Specific root length (SRL), mean root diameter of the fine-root system, and surface area and diameter of root tips of F. sylvatica (j), Q. petraea (r), P. abies (d) and P. menziesii (D) at different species richness levels. Different letters indicate significant differences among species richness levels within species. The species was labelled on the right side of the graphics, P < 0.05.

competitive ability index for all the possible mixed neighbourhoods indicated asymmetric belowground competition in favour of P. menziesii and P. abies. The significant differences of fine-root length density in ingrowth cores between different species at two sampling occasions, and the variation in CA values within species depending on the identities of neighbours, indicated that belowground competition may have occurred earlier than aboveground in this sapling stand. There may be several reasons responsible for this. On the one hand, the high planting density in this tree biodiversity experiment may have accelerated the interaction process between different species (Scherer-Lorenzen et al., 2005). On the other hand, it could be a reaction to potential interspecific competition, if the information-acquiring systems can detect the potential neighbouring species and the target plant produces more new fine roots in the mixed neighbourhoods (Aphalo and Ballare, 1995). It has indeed been shown that different plant species may identify co-occurring species, with higher root proliferation in ‘‘non-self’’ than in ‘‘self’’ neighbourhoods (de Kroon, 2007). Furthermore, this could also be the result of different cost/benefit strategies of co-occurring species in accordance with the optimal partitioning theory (Bloom et al., 1985; Kobe et al., 2010). The higher C investment in roots by the dominant coniferous species, P. menziesii and P. abies, may indicate that soil resources are more limiting than in the deciduous species. The inferior deciduous species, F. sylvatica and Q. petraea allocated more C aboveground, possibly to compete more effectively for light. The higher competitive strength of conifers in mixed neighbourhoods was also supported by higher RAI/LAI ratios in mixed versus pure species neighbourhoods. This belowground asymmetric competition was consistent with previous studies conducted in a mixed temperate forest, which is close to our site (Rewald and Leuschner, 2009a). However, cautions must be taken as fine-root growth was assessed in root-free soil patches represented by ingrowth cores. The different initial soil occupation intensities of the different species at this early stage of soil colonisation could also result in strongly different probabilities to grow fine roots in the unoccupied ingrowth cores. The fine-root prolongation rate, or recovery and

growth rate into the unoccupied soil patches, after severance during the ingrowth core installation, might be different from that in undisturbed soil. 4.2. Fine root morphological characteristics among different species Most morphological values measured here were consistent with those reported in previous studies. For example, SRL was similar to values reported for F. sylvatica (Grams et al., 2002), P. abies (Bolte and Villanueva, 2006), Q. petraea (Comas et al., 2002) and P. menziesii (Hendriks and Bianchi, 1995), respectively. Overall fine-root morphological characteristics were significantly different between the coniferous and deciduous trees. The thinner fine roots and higher SRL of the deciduous Q. petraea and F. sylvatica indicated higher soil exploitation efficiency, soil volume occupied per unit of structural C invested in fine roots, than in P. abies and P. menziesii. This greater exploitation efficiency may compensate to some extent for the apparent lower exploitation capacity. The results for fine-root morphology in different soil layers were consistent with those of previous studies showing that fine-root diameters tend to increase with soil depth (Bauhus and Messier, 1999; Wang et al., 2006). Surprisingly, this was also true for the fine roots growing in the homogenised ingrowth cores (data not shown), which might suggest that fine roots in different soil layers have different physiological functions (Wang et al., 2006; Leuschner et al., 2009). The difference tests showed that there were no significant differences between nutrient-enriched and untreated ingrowth cores for overall fine-root length density and surface area (P > 0.05). This was also true for fine-root length, surface area and morphological characteristics of each species at different species diversity levels, indicating that nutrient addition did not affect fine-root production, morphology and proliferation rates. It is generally assumed that a heterogeneous nutrient distribution, resulting from patchy nutrient input or local depletion by other species, is the main driver affecting the fine root proliferation, distribution and nutrient uptake strategies. However, no consistent patterns regarding the

P. Lei et al. / Forest Ecology and Management 265 (2012) 191–200

influence of nutrient enrichment on fine-root morphology have emerged so far. For example, it has been shown that nutrient enrichment can increase (Bakker et al., 2008), decrease (Ostonen et al., 2007b), or maintain SRL (Espeleta and Donovan, 2002; Guo et al., 2004; Tingey et al., 2005). The absence of any effect in our study may have been caused by the previous use of the site for agriculture, providing high background nutrient levels for the tree species used here. However, we did not analyse tissue nutrient concentrations, to confirm this. Another main objective of this study was to investigate how fine-root morphology of different species responded to interspecific competition. No significant differences in fine-root diameter and SRL were found between different species richness levels. This is in agreement with results from a natural, mature beech dominated forest (Meinen et al., 2009a). Instead, consistent and significant changes were detected in root tips. However, first order fine roots (roots tips) can be strongly colonised by ectomycorrhizal associations, which might alter the root tip diameter and surface area as well (Pergitzer et al., 2002; Guo et al., 2008). Therefore, it is difficult to attribute these root tip changes, e.g. increased root tip surface area and diameter of F. sylvatica and decreased root tip diameter of P. menziesii with increasing species richness, to morphological adaptation as a result of interspecific competition, or changes of mycorrhizal colonisation. The unchanged fine-root morphology of F. sylvatica, in conjunction with negative competitive ability (CA), demonstrated the low competitive ability of F. sylvatica that has been reported for mixed beech-spruce (Wang et al., 2001; Grams et al., 2002; Wang et al., 2003) and beech-Douglas fir stands (Hendriks and Bianchi, 1995) in early establishment stages. However, in other studies of fine-root competition in mature forest stands, F. sylvatica was the stronger competitor when compared to Q. petraea (Leuschner et al., 2001; Rewald and Leuschner, 2009a), to P. abies (Schmid, 2002; Bolte and Villanueva, 2006) and to P. menziesii (Reyer et al., 2010). It is not clear to what extent these different observations result from different stand ages and origins. Therefore, it would be interesting to find out, whether and when the competitive ability of co-occurring tree species in mixtures changes with increasing stand age. 5. Conclusions Mixing of up to four tree species did not increase the belowground soil occupation in a young, afforested stand. However, species that dominated aboveground were also the fastest to occupy new soil patches in ingrowth cores leading to size-asymmetric competition belowground. Hence, to maintain community composition in mixed-species stands beyond the immediate phase after planting, it may be advantageous to maintain larger distances between species with different above- and belowground growth rates, or to create patches, where individual plant are only exposed to intra-specific competition. Acknowledgements We are grateful to Ernst-Detlef Schulze, Max Planck Institute for Biogeochemistry, for the permission to use the BIOTREE experiment. We thank Renate Nitschke, Parvathi Venugopal, Adam Benneter, Germar Csapek, Julia Sohn and Alex Plum for assistance in the field and in the laboratory. Pifeng Lei received a scholarship from the German Academic Exchange Service (DAAD) and financial support from the University of Freiburg. References Aphalo, P.J., Ballare, C.L., 1995. On the importance of information-acquiring systems in plant-plant interactions. Functional Ecology 9, 5–14.

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