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Forest Ecology and Management 339 (2015) 5770

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Forest Ecology and Management


journal homepage: www.elsevier.com/locate/foreco

Forest restoration with Betula ssp. and Populus ssp. nurse crops increases
productivity and soil fertility
Hendrik Stark a,, Arne Nothdurft b, Joachim Block c, Jrgen Bauhus a
a

Chair of Silviculture, Faculty of Environment and Natural Resources, University of Freiburg, Tennenbacher Str. 4, 79085 Freiburg, Germany
Institute of Forest Growth, Department of Forest and Soil Sciences, University of Natural Resources and Life Sciences (BOKU), Peter-Jordan-Strae 82, 1190 Vienna, Austria
c
Department of Forest Monitoring and Environmental Care, Research Institute for Forest Ecology and Forestry Rhineland-Palatinate (FAWF), Hauptstrae 16, 67705
Trippstadt, Germany
b

a r t i c l e

i n f o

Article history:
Received 14 May 2014
Received in revised form 30 November 2014
Accepted 3 December 2014

Keywords:
Nurse crops
Populus ssp.
Betula ssp.
Biomass production
Nutrient cycling
Forest restoration

a b s t r a c t
The rapid re-establishment of forests following large disturbances is being seen as one option to increase
the contribution of forests to climate change mitigation. The temporary inclusion of pioneer trees as
nurse crops on disturbed sites can facilitate the establishment of target tree species and may additionally
benet productivity and soil fertility. In this study we compared productivity and nutrient cycling
between stands of oak target species (Quercus robur and Quercus petraea) that were established with
and without widely spaced Betula ssp. or Populus ssp. nurse crops. Simulation results for a full rotation
of oaks (180 years) indicated that both types of forests, with and without nurse crops, have a comparable
total productivity. However, stands with nurse crops supplied 5996 Mg ha1 harvestable biomass after
20 years, whereas the rst harvest of biomass from stands without nurse crops would occur at least
30 years later. Nutrient element costs associated with the removal of Betula ssp. wood were low compared to Populus ssp. Also, nurse crop stands had up to 2.5 times larger pools of exchangeable base cations
in top mineral soils (030 cm) compared to mono-specic oak stands. The high soil cation pools may have
resulted from reduced leaching under nurse crops or the increased recycling of cations, also from deeper
soil depth, via litter fall and ne-root turnover. Our results show that forest reestablishment with pioneer
tree species may be a suitable tool for the rapid recovery of forest productivity and mitigation potential
following disturbances while simultaneously helping to maintain or increase soil fertility.
2014 Elsevier B.V. All rights reserved.

1. Introduction
Climate change mitigation strategies in Europe aim to off-set
fossil fuels and replace energy-intensive materials with wood.
Therefore, the supply of biomass from forests is considered a crucial component within the set of renewable energy options
(Wiesenthal et al., 2006; Stupak et al., 2007).
However, during the last few decades the intensity and frequency of disturbances caused by storms, droughts, res, pest
insect outbreaks or wet snow events in central European forests
has risen measurably (Schelhaas et al., 2003; Nilsson et al.,
2004). Thus, approximately 16,000 ha or 0.15% of the total forest
area in Germany are annually disturbed considering the time
between 1950 and 2012 (EFI, 2013). At the European level such
Corresponding author. Tel.: +49 761 203 3678.
E-mail addresses: hendrik.stark@waldbau.uni-freiburg.de (H. Stark), arne.nothdurft@boku.ac.at (A. Nothdurft), joachim.block@wald-rlp.de (J. Block), juergen.
bauhus@waldbau.uni-freiburg.de (J. Bauhus).
http://dx.doi.org/10.1016/j.foreco.2014.12.003
0378-1127/ 2014 Elsevier B.V. All rights reserved.

disturbances are equivalent to 8% of the total annual fellings


(Schelhaas et al., 2003). Natural forest disturbances are thus a relevant aspect of central European forest management (Schelhaas
et al., 2003; Nilsson et al., 2004; Majunke et al., 2008; Mantau,
2012; Albrecht et al., 2013; Kraus and Krumm, 2013).
Pioneer trees could play a major role in the restoration of large
disturbed areas as they can possibly accelerate forest recovery and
therefore supply multiple benets for productivity and ecosystem
functioning (Alban, 1982; Man and Lieffers, 1999). Also, the cultivation of fast growing pioneer tree species such as Populus ssp.
or Betula ssp. (Bazzaz, 1979; Pommerening and Murphy, 2004)
may facilitate the adaptation of forests to environmental extremes
and simultaneously favor the rapid sequestration of atmospheric
carbon to mitigate climatic change (Messier et al., 2013; Brang
et al., 2014).
However, in forests managed on a selection basis or close to
nature, silvicultural systems with pioneers are typically avoided
in central Europe (Bauhus et al., 2013) in favor of those with
long-lived, commercially important tree species such as Fagus

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H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

ssp., Quercus ssp. or Picea ssp. Often, forest restoration with these
species is realized by planting mono-specic stands, which can suffer amongst others from late frost events in large forest openings
(Lundmark and Hllgren, 1987; rlander, 1993; Groot and
Carlson, 1996; rlander and Karlsson, 2000; Agestam et al.,
2003). Therefore, the capacity of forests to provide biomass may
be substantially reduced, if, following disturbances, regeneration
is delayed and thus productivity reduced (Osterburg et al., 2013).
On the other hand, large open areas in forests offer opportunities for new, alternative and more resistant silvicultural systems.
Hence, pioneer trees can be used as nurse crops, which are temporary mixtures of fast growing and light-demanding tree species in
the overstorey and shade-tolerant target tree species in the understorey (Pommerening and Murphy, 2004). During the initial years
of stand development, the pioneer trees facilitate the establishment of other tree species beneath their canopy. One possible
nurse effect is the rapid recovery of forest micro-climate and thus
the amelioration of environmental extremes, such as frost (Carlson
and Groot, 1997; Schmidt-Schtz and Huss, 1998). Outside of central Europe, nurse crops are therefore commonly used for large or
small scale reforestations (Pommerening and Murphy, 2004) following clearfelling (Keenan et al., 1995; Lieffers et al., 1996) or natural disturbances (Perala and Alm, 1990; Drouineau et al., 2000;
Vallauri, 2005; Nelson et al., 2012) and for the afforestation of
abandoned agricultural lands (Mander and Jogman, 2000;
Gardiner et al., 2004; Uri et al., 2007).
Once trees of the target species have been successfully established and start to suffer from inter-specic competition from
nurse trees, the latter are typically removed (Cotta, 1828;
Shepperd and Jones, 1985). Often, however, the nurse trees are just
killed and not commercially harvested, because it is feared that
their felling and extraction might damage the established regeneration of target species.
To ensure that this biomass of nurse trees is not wasted but
used, a new approach to establish widely-spaced nurse crops for
the purpose of woody biomass production has been developed
(Unseld et al., 2012). This approach is based on the assumption that
the temporary inclusion of fast growing pioneer tree species may
facilitate an early harvest of biomass and thus an earlier return
of investment of stand establishment costs to the land owner.
Additionally, the overall stand productivity may increase through
competitive reduction between tree species (Vandermeer, 1989;
Man and Lieffers, 1997) and thus a complementarity in resource
use, which typically occurs when mixing light demanding overstorey with shade-tolerant understorey trees (Man and Lieffers, 1999;
Richards et al., 2010; Forrester, 2014). To achieve this, nurse crops
are managed on rather short rotations and a wide tree spacing is
employed that facilitates harvesting of nurse trees with minimal
damage to the regeneration (Unseld et al., 2012).
Nurse crops may also improve nutrient cycling following forest
disturbances, when the situation is often characterized by high
mineralization rates of organic matter and reduced uptake of water
and nutrients. This can lead to high rates of leaching of nutrient
elements such as calcium (Ca), potassium (K), magnesium (Mg)
and nitrogen (N) and consequently a reduction in soil fertility
(Hornbeck et al., 1986; Hendrickson et al., 1989; Bauhus and
Bartsch, 1995; Yanai, 1998). These nutrient element losses may
be aggravated, if the sites are subsequently used for intensive production and harvesting of biomass in nurse crops and nutrients
contained therein (Sverdrup et al., 2006; Worrell and Hampson,
1997).
Owing to the rapid growth and canopy closure of pioneer tree
species, they have a higher nutrient and water uptake, thus reducing leaching, soil temperatures and mineralization rates, when
compared to slower growing tree species (Prescott, 2002). Interactions between nurse and target tree species may further accelerate

these processes and result in greater resource availability, uptake


and growth (Rothe and Binkley, 2001; Forrester, 2014).
While there have been many studies on the productivity or
nutrient cycling in mixed-species forests (Richards et al., 2010),
we are not aware of any studies that have focussed on temporary
mixtures of target species such as Quercus ssp., Fagus ssp. or other
with Populus ssp. or Betula ssp.
Therefore, the rst objective of this study was to assess whether
forest restoration with widely spaced nurse crops can facilitate
early biomass harvests, increase the overall stand productivity,
and whether it thereby also intensies harvest-related exports of
nutrient elements such as Ca, K, Mg, N, and P when compared to
conventional restoration of forest stands with the target species
Quercus robur and Quercus petraea. The second objective was to
study possible effects such nurse crops may have on ecosystem
nutrient cycling. Thus, we hypothesize that nurse crops of broadleaved pioneer tree species can buffer disturbance-induced and/
or harvest-related reductions in soil fertility. Additionally, the
study also investigated options to reduce harvest-related nutrient
costs in nurse crop systems. For this purpose, the nutrient costs
of biomass harvest from Populus ssp. or Betula ssp. were compared
with those of several other important tree species and at different
harvesting intensities. Thus, this study is the rst to examine productivity as well as nutrient cycling and conservation in widely
spaced, short-lived Populus ssp. or Betula ssp. nurse crops, providing the foundation for the short-term sustainable production of
woody biomass from disturbed forest areas in central Europe.

2. Materials and methods


2.1. Study area and trial forests
This study was carried out in the German federal state of Rhineland-Palatinate. Here, nurse crop trials were established in 1991
following large scale wind throw of Picea abies (L.) Karst. The trials
originally aimed to study the effects of nurse crops of pioneer tree
species on the survival, growth and quality of site adapted target
tree species such as oak (here: Quercus robur and Quercus petraea)
when planted at water logged sites under open eld conditions.
Thus, the trials included oak stands planted as conventional monocultures and oak stands that were planted under a sheltering nurse
crop of pioneer tree species (Schmidt-Schtz and Huss, 1998).
Treatments were randomly assigned. Between 1991 and 1998
weed was controlled manually, dead tree saplings were replaced
and naturally regenerated trees were removed. Between 20% and
70% of the nurse tree seedlings died between 1991 and 1994 and
were replaced in 1994 (Schmidt-Schtz and Huss, 1998).
For the purpose of this study, we used two of the original trials,
Kirchberg (N 49.98, E 7.32; 450 m a.s.l.) and Sobernheim
(N 49.86, E 7.69; 420 m a.s.l.), for soil and biomass sampling in
2011. We selected 16 plots equally spread across both trials (study
sites). Hence, we selected eight plots with oak monoculture and
eight plots with oak growing under a nurse crop shelter (Fig. 1).
Among the plots selected in Kirchberg, two were originally
established as nurse crops with Populus tremula L. x Populus tremuloides Michx. Astria and two were established as nurse crops with
Betula pendula Roth x Betula pubescens Ehrh. Quercus robur L. was
the original target species in Kirchberg. It was used to establish
the mono-specic oak plots as well as the understorey of nurse
crop plots. In Sobernheim two plots were established as nurse
crops with Populus tremula L. x Populus tremuloides Michx. Astria
and two as nurse crop with Betula pendula. The target tree species
here was Quercus petraea (Mattuschka) Liebl., which was likewise
planted in monocultures as well as in the understorey of nurse
crops. In our statistical analyses we examined whether the

H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

59

specic oak plot in Kirchberg and two mono-specic oak plots in


Sobernheim were planted at 2  1 m.
Stand densities remained constant in aspen-oak and birch-oak
stands because individuals that had died were replaced until
1998. In mono-specic oak plots the stand densities successively
decreased due to self thinning. Thus, the mean stand density in
mono-specic oak stands in Kirchberg was 7743 stems per hectare
(N ha1) in 1991 and 4814 N ha1 in 2011; in Sobernheim stand
densities were 7130 N ha1 in 1991 and 5127 N ha1 in 2011.
Mean diameters at breast height of aspen and birch were 19.4
and 17.9 cm in Kirchberg and 16.9 and 17.4 cm in Sobernheim;
mean heights were 15.5 and 12.9 m in Kirchberg and 13.8 and
10.9 m in Sobernheim, respectively. Understorey oaks were about
2.42.5 cm in diameter at breast height and 3.63.9 m high.
Mono-specic oaks in Kirchberg were on average 7.5 cm in diameter at breast height and 9 m high; in Sobernheim they had a mean
diameter at breast height of 5.8 cm and were 7.7 m high.
The plots were mostly square in shape with an edge length of
25 m in aspen-oak, 50 m in birch-oak and 25 or 50 m in mono-specic oak stands. Plots in Kirchberg were fenced in 1994 while only
a central 5  5 m square was fenced within each plot in
Sobernheim.
The soils at both study sites originate from historical loess
deposits mixed with clay and sand stone gravels and have a water
impermeable layer at 3050 cm below the surface. Thus, the Kirchberg site was dominated by Pseudogley and the site in Sobernheim
was dominated by Cambisol-Pseudogley. Mean air temperatures
(19882011) during the vegetation season (daily average > 5  C,
AprilOctober) were 12.4 and 13.0  C with a mean precipitation
(2002 until 2011) of 552.9 and 423.5 mm in Kirchberg and Sobernheim (FAWF, 2013), respectively.
2.2. Element pools in soil and biomass

Fig. 1. Chart of the study sites Kirchberg and Sobernheim as originally established
in 1991 (modied from Schmidt-Schtz and Huss, 1998). The set of plots with
mono-specic oak (oak-mono), aspen-oak and birch-oak stands assessed in the
present study were marked with bold lines and color codes.

difference with respect to tree species selection had any effect on


the nutrient cycling or the nutrient costs of biomass harvest. If
such effect was present, xed intercept parameters were estimated
and further applied in the statistical modeling.
In the following we will refer to all Quercus ssp. plots that were
established with a Populus ssp. nurse crop as aspen-oak. Quercus
ssp. plots that were established under a Betula ssp. nurse crop were
referred to as birch-oak. The aspen or birch layer of these plots
will be simply called aspen and birch, although in most cases
hybrids were used. Oak monocultures will be referred to as
mono-specic oak in text and as oak-mono in gures and tables.
The understorey oak was planted in 1996, while aspen in aspenoak plots, birch in birch-oak plots and mono-specic oak plots
were planted in 1991. In 2011 the aspen and birch nurse crop trees
were nally harvested, thereby releasing the understory oak trees
from intensive competition.
Plant spacing for aspen or birch was generally 4  4 m. Understorey oaks in Kirchberg were planted at 4  1 m and understorey
oaks in Sobernheim were planted at 4  1.5 m and in accordance
with regional silvicultural practices, respectively. Oak rows planted
under nurse crops were aligned parallel to the nurse crop rows and
offset by 2 m. Spacing in mono-specic oak stands was 1.5  0.7 m
in three out of four mono-specic oak plots in Kirchberg and in two
out of four mono-specic oak plots in Sobernheim. One mono-

To determine relevant base cation pools in forest oor and mineral soils, soil cores were collected from 12 randomly selected sampling positions per plot. We used larger cylinders for the forest
oor ( 170 mm) and smaller ones for the mineral soil (
50 mm). Mineral soil cores were divided into 010 and 1030 cm
depth layers. To obtain information from a greater soil depth, additional samples were collected from 3070 cm ( 24 mm) at four
out of 12 sampling positions. Samples were oven dried at 40  C
and their individual dry weight was recorded.
Subsequently, to reduce laboratory costs, pairs of samples
were bulked to yield six samples (two samples for the layer
3070 cm) per layer and plot. These bulked samples were sieved
(2 mm), ground and 25 ml of 1 M NH4Cl were used to extract
exchangeable base cations from 2.5 g soil sub-samples. We used
the mass of ne soil per unit of sample volume multiplied by
the respective nutrient element concentration to estimate nutrient element contents per sample volume and subsequently per
area. Likewise, forest oor samples were mixed, sub-samples
were ground to powder and subsequently digested in 65%
HNO3 at 190  C (pressure vessels, Loftelds Analytical Solutions,
Neu-Eichberg, Germany). The diluted solutions from extractions
and digestions were analyzed for element concentrations using
ICP-OES (Spectro, Kleve, Germany) (Knig, 2005). Organic carbon
(C) and nitrogen (N) concentrations were measured using dry
combustion (Truspec, Leco, St. Joseph, USA). Soil pH was measured in CaCl2.
To determine base cation pools within the woody biomass, at
each plot and for each tree species ve trees were destructively
sampled across the entire range of all tree diameters at breast
height, respectively. Diameter at breast height (cm) and tree height
(m) were recorded immediately after felling, and stem discs were
extracted at 2 m intervals along aspen and birch stems. The length

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H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

of oak stems with a diameter larger than 4 cm was divided into six
equally long sections and stem discs were extracted at these relative intervals. From each sample tree with a diameter at breast
height thicker than 4 cm three branches were sampled from the
lower, middle and upper crown section, respectively. Subsequently, the fresh weight of all remaining branches and stem sections was recorded. Stem disc fresh weight was recorded
separately for wood and bark. Oak trees with a diameter at breast
height thinner than 4 cm were assigned to the branch compartment (Stark et al., 2013).
For element analysis, wood shavings of stem discs were collected from two perpendicularly cross-sectional transects while
stem bark fragments were chipped. Both types of sub-samples
were oven dried at 40  C until constant weight, mixed at the tree
level, and ground. Likewise, sample branches were chipped, mixed
at the tree level and ground. Finally, compartment-specic element
analysis was undertaken as described above for forest oor
samples.
The respective compartment-specic aboveground woody biomass of all trees was estimated using allometric biomass equations
(Stark et al., 2013). The species-specic biomass of roots between 2
and 5 mm was measured using the soil cores (0 and 30 cm depth)
collected for this study, while the biomass of roots larger 5 mm and
stumps was estimated according to equations provided in Wang
(2006). The biomass of birch regeneration with diameters at breast
height ranging between approximately 1 and 5 cm was estimated
using equations from Uri et al. (2007). The nutrient element pools
contained within sample tree stem wood, stem bark and branches
were nally calculated using the measured compartment-specic
biomass and element concentrations.
We did not measure nutrient element concentrations in understorey birch regeneration. In order to estimate the nutrient element pools within the aboveground woody biomass of birch
regeneration we used the concentrations measured in sample tree
branches, assuming that the stem-wood to stem-bark ratio and
thus the nutrient element concentrations both in sample branches
of nurse crop trees and birch regeneration were comparable. Also,
we did not measure nutrient element concentrations in roots.
Therefore, we used information provided in the literature to infer
the average ratio between nutrient element concentrations in tree
branches and roots. Based on such comparisons, we assumed tree
roots with diameters between 2 and 5 mm to have comparable
nutrient element concentrations as measured in our sample tree
branches (Jacobsen et al., 2003), and we assumed stumps and roots
>5 mm to have 50% of these branch concentration (Rademacher,
2005; Block et al., 2007).
For planted aspen and birch in aspen-oak and birch-oak plots
Pn
we calculated the biomass and nutrient
element pools per ha on
t
j1 j
each sample plot separately as nab
 10; 000, with t j being the
single tree biomass or nutrient element pool of each planted aspen
and birch tree on a specic plot, and a and b being the width of the
regular plant spacing in x and y direction. The biomass and nutrient element pools per ha of mono-specic oak, natural regeneration and understory oaks were estimated by means of 2 m wide,
diagonal transect samples.

2.3. Nutrient element costs of wood

2.4. Statistical analysis


Linear mixed-effect models were employed to analyze how
aspen-oak and birch-oak plots may affect soil base cation and carbon pools when compared to mono-specic oak plots. This modeling approach accounted for the nested study design and the
partially unbalanced data set. Because the data were skewed to
the right, a log-transformation was applied prior to model tting.
We used dummy variables and indicator functions to incorporate
categorical groups of xed effects such as treatment, soil depth
and study site. Generally, non independence of predictor variables
was tested and 0.7 was used as threshold for the correlation coefcient (Dormann et al., 2013).
2.4.1. Modeling of soil nutrient element pools
The full models were of the form
1
1
Wijklm b1
0 b1  I ftreat g b2  Ifdepthg
1

b3  Ifsite Sobernheimg
1

b4  Iftreatg  Ifdepthg  Ifsite Sobernheimg


1

b5  Iftreatg  Ifsite Sobernheimg


1

b6  Iftreatg  Ifdepthg
1

b7  Ifsite Sobernheimg  Ifdepthg bijkl ijklm ; 1






with bijkl  N 0; j2 and ijklm  N 0; k2 . Wijklm was the logarithmic
element pool of soil sample m of treatment i, soil depth j and study
1
site k from plot l. b0 denoted the intercept of the full model representing pools in the forest oor under aspen-oak stands in Kirch1
1
berg and b4 to b7 denoted interactions among the main xed
effects. bijkl was a plot level random effect and ijklm denoted the
residual error. The 0-hypothesis H0 : b1
0 meaning that a paramr
eter br1 equals 0 was tested using Wald-tests. Model selection was
done using the likelihood based information criterions AIC and BIC.
2.4.2. Modeling the nutrient element costs of biomass removal
For assessing the nutrient element costs of wood as a function
of tree species and biomass compartment and using log-transformed data we tted similar models
2
2
Pijklm b2
0 b1  I ftreat g b2  I fsite Kirchberg g
2

b3  Ifcompartmentg b4  Iftreat g  Ifcompartmentg


2

b5  Iftreatg  Ifsite Kirchberg g bijkl ijklm :

Pijklm represented the logarithmic biomass removal per mass unit of


the respective nutrient element of sample tree m under treatment i
2
of biomass compartment j and at study site k from plot l. b0 denoted
the intercept of the full model representing the amount of stem
wood (kg) biomass that can be removed per unit nutrient element
(kg) from oak trees (mono-specic stands) in Kirchberg.
2.4.3. Modeling of cation exchange capacity
To assess, whether differences in soil exchangeable cation pools
between treatments may be caused by changes in the quantity or
quality of organic matter, we tted a third model. Because the data
were skewed to the right a log-transformation of response and predictor variables achieved the best model t. The model was
3
3
3
Hijkl b3
0 b1  logCcon b2  logpH b3  Iftreatment g

We interpreted the woody biomass (kg) divided by the amount


of a nutrient element contained therein (kg) (Pastor et al., 1984;
Wang et al., 1991) of aspen and birch sample trees as the nutrient
element costs of woody biomass harvest. Additional data for several other tree species of major economic importance were provided by Pretzsch et al. (2013) or compiled from Jacobsen et al.
(2003) for comparison.

b4  logCcon  Iftreatmentg bijkl ijklm :

Hijk was the logarithmic cation exchange capacity of soil sample k of


3
treatment i and plot j. The intercept b0 represented the logarithmic
cation exchange capacity at a given logarithmic soil organic carbon
concentration and logarithmic pH (CaCl2) in mineral soils to 10 cm
depth under mono-specic oak stands.

H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

2.5. Modeling of early biomass and related nutrient element pools


There is very little information on the sequestration of nutrient
elements in biomass of young forests during their establishment
phase. However, during this period the rapid uptake of nutrients
into tree biomass could substantially reduce nutrient leaching. To
compare nutrient element sequestration from the time of stand
establishment until age 20 years, diameter, height and survival
were recorded for individual trees of selected sample rows in ve
mono-specic oak plots and for all aspen and birch individuals
on four aspen-oak and birch-oak plots (Schmidt-Schtz and Huss,
1998; Eggert, 2006). This resulted in plot mean diameters, heights
and stand densities available for the years 19911997, 2006, 2011.
We then estimated diameters, heights and densities for all years
in which these variable had not been recorded. For this, we pooled
the plot means from all years in which data had been recorded and
drew 199 sub-samples with replacement from this data pool, each
comprising 15 values per species and study site, respectively. For
each sub-sample we tted Pettersons (1955) growth function for
the plot mean tree diameter at stem base versus stand age, and
used these models to predict the successive development of plot
mean diameters of each treatment between the time of establishment and age 20 years.
For each predicted mean diameter, the respective biomass was
estimated using specic allometric biomass equations (Stark et al.,
2013) and was then multiplied by the number of trees per hectare.
For nurse crop systems a constant stand density was assumed. For
pure oak stands we regressed measured mean stand density values
against mean diameters using a polynomial regression model and
subsequently estimated the consecutive annual stand density
development. We used nutrient element concentrations measured
during the eld work in 2011 to calculate nutrient element pools.
For each of the 199 sub-samples the entire procedure was gradually calculated to ensure continuous error propagation.
2.6. Modeling and predicting long term development of biomass and
nutrient element pools
We also predicted the annual biomass and nutrient element
pools for oaks established with and without aspen and birch nurse
crops between stand age 20 years and the end of their rotation period. For this we used a single tree, distance-independent growth
modeling approach. Our model specication aimed to reproduce
the local management concepts for oak quality wood production.
In brief, such concepts rely on initially high stand densities and
the canopy is generally kept close for three to four decades following canopy closure to ensure self-pruning for the production of
high quality timber. Once the targeted branch free bole length is
reached, selection thinning is used to release potential future crop
trees from competition to stimulate their crown expansion and
diameter growth (Dong et al., 2007; Spiecker, 2007).
We simulated complete data representing the oak trial plots
within the model according to their original stand density and
age. Oak stands established under an aspen or birch nurse crop
were simulated according to their physiological age, which was
derived by matching their actual height at the time of release with
the age-specic yield table tree height. Finally, a diameter at breast
height was assigned to each oak from prior distributions.
Algorithms for tree growth, thinning and harvesting were
adopted from the WEHAM tree growth simulator (Bsch, 2013).
In WEHAM, an annual diameter increment is assigned to each tree
according to its diameter at breast height at a given reference age,
and following Slobodas (1971) growth function. The increment is
then used to obtain a diameter prognosis for the subsequent simulation cycle. Tree height was inferred from each predicted diameter using Pettersons (1955) growth function. All model

61

parameters were derived from model ts to forest inventory data


collected in the federal state of Rhineland-Palatinate (Bsch, 2013).
To conform with current management practices, once the modeled oaks exceeded a height of 12 m, a beech (Fagus syilvatica)
understorey was introduced into the model using age specic
information on tree diameters, their distribution as well as stand
density provided in Grote (2003) and Mnder (2005). Beech height
growth was modeled according to data collected from understorey
beech in the German national forest inventory (BMELV, 2002). The
above described approach provided reliable predictions for growth
of beech trees older than approximately 30 years. If not stated
otherwise, model results comprise the biomass and nutrient element pools of both oak and beech.
Following the removal of aspen and birch trees, we assumed a
ve-year release effect for oaks established under aspen and birch
nurse crops. This effect was depicted as an annual increase of 8%
over the originally predicted diameter increment at breast height
and lasted for a period of 5 years. This resulted in an annual diameter increment of 36 mm, which was in accordance with data
reported by Nutto (1999) for widely spaced (3  0.7 m) young
oak trees. The respective ability of oak to temporarily increase its
diameter increment following release was demonstrated by
Utschig and Pretzsch (2001).
Based on diameter estimates, the total aboveground woody biomass was predicted using allometric biomass equations developed
by Stark et al. (2013) for oaks with diameter at breast height
between 011 cm, by Zell (2008) for oaks thicker than 11 cm and
by Grote (2003) for beech. Total aboveground woody biomass of
oak was then subdivided into stem wood and bark as well as the
wood and the bark of branches thicker and thinner than 70 mm
using relative proportions of the total aboveground woody biomass
according to data published by Andr et al. (2010). Compartmentspecic nutrient element pools for oak were calculated using concentrations for wood, bark and branches determined in this study;
concentrations for beech were adopted from Rademacher (2005).
Thinnings from below were conducted until the age of
100 years. Older oak stands were selectively thinned, and the thinning intensity was inferred from the difference between the modeled basal area and yield table values (FVA-BW, 2000). Model
internal thinning intervals varied between nine and 10 years irrespective of practical silvicultural treatments, but the total removals
were assumed to be in accordance with best forest management
practice in Germany. The selection of trees to be removed was
based on a diameter-dependent criterion (Bsch, 2013) combined
with a random selection process. Beech individuals were removed
latest once they exceeded 70% of mean oak height to prevent interaction with oak crowns. Harvesting was simulated as a clearfelling
operation once the mean oak diameter of 70 cm was reached but
latest at the age of 180 years.
Until a stand height of 17 m thinned trees, and thus biomass
and nutrient elements contained therein, were assumed to remain
in the stand. Once the critical height of 17 m was reached, a branch
free bole length of 10 m a requirement for the production of high
grade oak wood was assumed for selected target trees due to
competition induced self-pruning (Spiecker, 2007). The biomass
and nutrient element removals associated with thinnings applied
beyond the mean height of 17 m were therefore considered to be
removed from the stand. Possible random variation of the model
predictions was examined using a Monte-Carlo Simulation with
199 iterations.
2.7. General statistics
Multiple pair-wise comparisons of means between treatments
(biomass and soil element concentration and pools; base cation
saturation, pH and medium root abundance in soil; nutrient

H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

3.1.1. Past development of biomass and related nutrient element pools


We reconstructed the past development of biomass and related
nutrient element pools for all treatments. According to this analysis and based on the interpretation of 95% condence intervals, the
biomass accumulated in aspen, birch, and mono-specic oak
stands in Kirchberg was comparable throughout the initial
20 years of stand life (Fig. 3 left panel). In Sobernheim, the 95%
condence intervals indicated signicantly larger biomass pools
in birch than in aspen and mono-specic oak stands between the
ages of 10 and 15 years; no signicant differences were observed
for the time before and after that period.
The corresponding Ca, K and Mg pools (Figs. S1 and S2), element
concentrations measured in 2011 Tables S7 and S8in Kirchberg
were signicantly lower in birch than in aspen or mono-specic
oak between the ages 15 and 20 years, respectively. No differences
were observed for P and N. Also, Ca pools in mono-specic oak

biomass
Ca

100

50

50

300

300

150

150

K
Mg

200

200

100

100

60

60

30

30

300

300

150

150

40

40

20

20

birch
underst. oak

aspen
underst. oak

oakmono

birch
underst. oak

aspen
underst. oak

After two decades, the mean aboveground woody biomass


yielded by aspen, birch and mono-specic oak plots in Kirchberg
was 96 (30), 79 (8) and 95 (30) Mg ha1 (numbers in parentheses
indicate standard deviations), respectively. The biomass produced
by these different stand types in Sobernheim was 67 (0.3), 59 (5)
and 49 (18) Mg ha1, respectively (Fig. 2, Tables S1 and S2). In Kirchberg oaks growing in the understorey of aspen-oak plots comprised 4.8 (0.1) Mg of biomass per ha and those growing in
birch-oak plots had 4.5 (0.1) Mg ha1; in Sobernheim understorey
oaks contributed 2.7 (0.2) Mg ha1 to the overall biomass in
aspen-oak plots and 2.7 (0.02) Mg ha1 in birch-oak plots.
Mean Ca, K, Mg, N and P pools in understorey oaks in Kirchberg
were 12 (1.5), 9 (1), 2 (0.3), 17 (2) and 1.5 (0.2) kg/ha and 7 (0.1),
4.5 (0.1), 1 (0), 10 (0.2) and 1 (0) kg/ha in Sobernheim. Detailed
information on biomass and nutrient element pools in roots,
stumps and natural regeneration are presented as Supplementary
material in Tables S1S6.
Multiple pair-wise comparisons of the above mean biomass and
nutrient element pools did not consider possible study site effects
because of the low number of aspen-oak and birch-oak replicates
per study site. The tests indicated no signicant differences in
the biomass pools among aspen-oak, birch-oak and mono-specic
oak, irrespective of whether the oak understorey was considered in
aspen-oak and birch-oak plots or not. K pools were signicantly
larger in aspen compared to birch and P pools were signicantly
larger in aspen compared to mono-specic oak. No signicant differences among the treatments were found for Ca, Mg and N.

100

oakmono

3.1. Productivity and related nutrient element pools in biomass


20 years post establishment

Sobernheim

3. Results

Kirchberg

biomass [Mg/ha] and nutrient [kg/ha] pools

element costs of wood) were performed following the hypothesis


that their means were not signicantly different from 0 using the
a 0:05 level. In order to account for unequal samples sizes the
tests were performed according to the generalized linear hypothesis using the glht function of the multcomp library in R (Hothorn
et al., 2008; Bretz et al., 2010) and were based on generalized linear
models. Comparing the nutrient element costs of wood among several tree species in central Europe we assumed a gamma data distribution and specied models with a log-link function between
predictor and response. In all other cases, a Gaussian data distribution with an identity-link function was assumed and, if necessary,
data were log-transformed prior to model tting. We used the programming language and statistics environment R version 2.12.0 (R,
2010) including MASS (Venables and Ripley, 2002), nlme (Pinheiro
et al., 2011) and RODBC (Ripley and Lapsley, 2011) library.

62

Fig. 2. Empirical aboveground woody biomass and nutrient element pools


contained therein displayed for aspen nurse crops and their understorey oak
(underst. oak), birch nurse crops and their understorey oak and mono-specic oak
(oak-mono) in Kirchberg and Sobernheim, respectively. Only the biomass of aspen
and birch nurse crops was actually harvestable at the age of 20 years. Understorey
oaks would continue growth following the nurse crop removal. Error bars indicate
standard deviations among the plots of each study site. Multiple pair-wise
comparison of means across both study sites indicated no signicant differences
in the biomass pools among aspen, birch and mono-specic oak. K pools were
signicantly larger in aspen compared to birch and P pools were signicantly larger
in aspen compared to oak-mono. No signicant differences among the treatments
were found for Ca, Mg and N. Mind: left and right axes display the same scales and
units.

were signicantly larger than in aspen. In Sobernheim P pools in


birch were larger than in aspen or mono-specic oak between
the ages 10 and 15 years.
Oaks growing in the understorey of aspen or birch could not be
considered in this analysis. At the age of 20 years, understorey oaks
contributed approximately 3 Mg ha1 to the overall stand biomass.
Likewise, root, leave and grass biomass was not considered.
3.1.2. Future development of biomass and related nutrient element
pools
We also estimated the future development of biomass and
related nutrient element pools in oak plots that were established
with and without nurse crops (Figs. 3 right panel, S1 and S2).
Please mind that aspen and birch were harvested from aspen-oak
and birch-oak plots at the age of 20 years.
According to our model simulations and depending on the measured, local stand parameters in 2011, oak stands that were established as mono-specic oak would reach a mean stand height of
17 m and thus the starting time of commercial thinning at the
age of 54 years in Kirchberg and 70 years in Sobernheim. Oak
established in aspen-oak or birch-oak stands would reach that
height at the age of 73 years in Kirchberg and 78 years in Sobernheim (Tables S9S12).

63

H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

Sobernheim
Kirchberg
biomass [Mg/ha]

The biomass reduction due to mortality or release of future crop


trees or cutting of wolf trees prior to commercial thinning would
be 188 and 143 Mg ha1 in oak plots established as mono-specic
oak in Kirchberg and Sobernheim and 113 and 61 Mg ha1 in oak
plots that were established as aspen-oak or birch-oak in Kirchberg
and Sobernheim, respectively (Figs. 3, S1 and S2 right panel, Tables
S9S12). Nutrient element returns will follow a similar pattern
according to their respective concentrations.
The mean annual increment of stand height and diameter at
breast height in mono-specic oak stands would be 0.20 m year1
and 0.44 cm year1 in Kirchberg and 0.16 m year1 and
0.37 cm year1 in Sobernheim; the mean annual increment of
height and diameter at breast height in oaks stands established
in aspen-oak or birch-oak plots would be 0.17 m year1 and
0.38 cm year1 in Kirchberg and 0.16 m year1 and 0.34 cm year1
in Sobernheim.
The biomass removal by thinning of competing oaks and beech
understorey trees in mono-specic oak stands would yield on average 4.8 Mg ha1 year1 in Kirchberg and 4.5 Mg ha1 year1 in
Sobernheim, and 4.6 Mg ha1 year1 and 4.4 Mg ha1 year1 would

Table 1
Total biomass and nutrient element removals from mono-specic oak stands and
aspen-oak and birch-oak stands in Kirchberg and Sobernheim. In all cases the biomass
produced by a beech understorey is included, too.
Site

Treatment

Biomass

Ca

Mg

Oak-mono
Aspen-oak
Birch-oak

Mg/ha
898
928
911

kg/ha
1733
1896
1746

kg/ha
1291
1362
1286

kg/ha
255
271
257

kg/ha
1748
1871
1841

kg/ha
127
152
144

Oak-mono
Aspen-oak
Birch-oak

823
828
820

1643
1728
1651

1259
1313
1234

203
216
202

1773
1855
1814

122
137
131

be yielded by oak stands planted in aspen-oak or birch-oak plots in


Kirchberg and Sobernheim, respectively (Figs. 3 and 4).
At the time of nal harvest the mean diameter at breast height,
the mean height and the stand density of oak stands established
without nurse crops would be 71 cm, 30 m and 72 trees per ha
in Kirchberg and 65 cm, 30 m and 92 trees per ha in Sobernheim.
The mean diameter at breast height, the mean height and the stand

350
300
250
200
150
100
50
350
300
250
200
150
100
50

100
80
60
40
20
0
100
80
60
40
20
0

ci 0.0250.975
aspenoak mean
birchoak mean
oakmono mean
ci 0.0250.975
oaknursecrop mean
oakmono mean

10

15

20

50

100

150

stand age [years]

cumulative removal [Mg/ha]


biomass

Fig. 3. Left panels: Reconstructed aboveground woody biomass development of aspen, birch and mono-specic oak (oak-mono) stands between the ages 0 and 20 years at
both study sites, respectively. Mind that the biomass of understory oak could not be included here. They contributed about 3.2 Mg biomass per ha at the age of 20 years. Right
panels: Biomass development of oak stands established with (black) and without (red) a nurse crop. These pools include a beech understorey, which is commonly installed to
suppress the development of epicormic branches in oak stems. Mind that the age of oaks established without a nurse crop corresponds to the stand age given at the x-axis,
while oaks established with a nurse crop were ve years younger. For details please refer to the Supplementary Tables S9S12. Presented are means and 95% condence
intervals of 199 model iterations. (For interpretation of the references to color in this gure legend, the reader is referred to the web version of this article.)

Kirchberg

Sobernheim

1000

1000
aspenoak

800

birchoak

800

600

oakmono

600

400

400

200

200

0
0

50

100

200 0

50

100

200

age [years]
Fig. 4. Cumulative biomass removals derived from three exemplied model runs for aspen-oak, birch-oak and mono-specic oak stands across the complete rotation period.
Included is a beech understorey, which would be introduced at the oak height of 12 m to prevent epicormic branches in oak stems. For details please refer to the
Supplementary Tables S9S12.

64

H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

Ca [mg/g]

12
10
8

ab
a

6
4
2
birchoak

aspenoak

oakmono
4.0

pH CaCl2

3.8

3.4
3.2

birchoak

aspenoak

oakmono

50

40

20

birchoak

aspenoak

10
oakmono

base cation saturation [%]

Fig. 6. Soil acidity (pH) measured in mineral soils in 010 cm depth under aspenoak, birch-oak and mono-specic oak (oak-mono) plots. Different letters indicate
signicant differences between treatments and were produced from multiple pairwise comparisons of means.

30

140
130
120
110
100
90
oakmono
aspenoak
birchoak

80
70

Fig. 5. Ca concentrations measured in the forest oors of aspen-oak, birch-oak and


mono-specic oak (oak-mono) stands. Different letters indicate signicant differences between treatments and were produced from multiple pair-wise comparisons of means.

3.6

CEC [molc/g soil] at pH 3.4

14

Fig. 7. Base cation saturation of the exchange complex as measured in the mineral
soil in 010 cm depth aspen-oak, birch-oak and mono-specic oak (oak-mono)
plots. Different letters indicate signicant differences between treatments and were
produced from multiple pair-wise comparisons of means.

40

60

80

100

120

C [mg/g soil]
Fig. 8. Regression curves for cation exchange capacity (CEC) dependent on the
organic carbon concentration in the mineral soil in 010 cm depth (Eq. (3)). The pH
(CaCl2) is xed at its overall mean of 3.4.

density of oak stands established with nurse crops would be 66 cm,


30 m and 88 trees per ha in Kirchberg and 58 cm, 20 m and 112
trees per ha in Sobernheim. These values represent the oak layer
only; values for the respective beech layer are listed separately
in Tables S9S12.
Over the complete rotation period of 180 years, a total amount
of 898 and 823 Mg ha1 biomass (including oak and beech biomass) would be harvested from oak stands established without
nurse crop in Kirchberg and Sobernheim, respectively. In contrast,
832 and 761 Mg ha1 biomass would be harvested from oak stands
established under aspen or birch nurse crop in Kirchberg and
Sobernheim, respectively. Adding the biomass produced by aspen
and birch to these values would yield in total 928 Mg ha1 from
aspen-oak and 911 Mg ha1 from birch-oak stands in Kirchberg;
828 Mg ha1 would be harvested from aspen-oak and 820 Mg ha1
from birch-oak in Sobernheim (Table 1 and Fig. 4).

3.2. Nutrient element pools in soils 20 years post establishment


Ca concentrations in the forest oor beneath aspen-oak plots
were signicantly higher than in mono-specic oak plots (Fig. 5,
Tables S13 and S14), whilst no signicant differences among treatments were found for K, Mg, N and P. The pH (Fig. 6) in the surface
mineral soil (010 cm) was signicantly higher in aspen-oak and
the saturation of base cations (Fig. 7, Tables S13 and S14) was signicantly higher in both aspen-oak and birch-oak than in monospecic oak plots.
Additionally, model (3) analyzing the cation exchange capacity
as a function of soil organic carbon (C) concentration as well as
the nurse crop treatment and their interactions revealed the signicance of all these effects within the upper 10 cm of mineral soil
(Table S15). These results suggest a different quality of organic
matter with a higher increase in cation exchange capacity per unit
organic carbon in soils under aspen-oak and birch-oak than under
mono-specic oak (Fig. 8).
Finally, the pools of exchangeable Ca in the top 10 cm mineral
soil were 175 (101), 130 (112) and 62 (48) kg ha1 in aspen-oak,
birch-oak and mono-specic oak plots in Kirchberg and for the
same treatments in Sobernheim 177 (67), 131 (47) and 96
(28) kg ha1, all signicantly larger in aspen-oak and birch-oak
than in mono-specic oak stands (Fig. 9, Tables S3 and S4).
Exchangeable K pools in aspen-oak, birch-oak and mono-specic oak plots were 76 (21), 68 (19) and 52 (12) kg ha1 in Kirchberg and 79 (16), 55 (8) and 51 (9) kg ha1 in Sobernheim,
respectively. In Kirchberg both the K pools in aspen-oak and
birch-oak were signicantly larger compared to mono-specic

C*1000

H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

Kirchberg

Sobernheim

measured predicted
[kg/ha]
[%]

measured predicted
[kg/ha]
[%]

100

400

100

400

50

200

50

200

Ca

1200

1200
400

600

400

600

200
0
1000

200
0
1000

400
500

400
500

200

Mg

0
700

400

350

200
0
700

400

350

200
0

oakmono
aspenoak
birchoak

oakmono
aspenoak
birchoak

400

8000

400

200

4000

200

oakmono
aspenoak
birchoak

4000

200

oakmono
aspenoak
birchoak

0
8000

65

forest floor

min. soil 010 cm

min. soil 1030 cm

min. soil 3070 cm

Fig. 9. Left bar triplet of each panel: Measured nutrient element pools per soil
depth layer with standard deviations (error bars) given for the overall element pool
of all depth layers, respectively. Right bar triplet of each panel: To increase the
visibility of treatment effects, the relative difference between the treatment aspenoak and the mono-specic oak reference stand as well as the relative difference
between the treatment birch-oak and the mono-specic oak reference stand was
calculated from layer-specic nutrient element pool predictions using signicantly
parametrized models (1). Thus, for each depth layer (for each shade of gray) the
element pool under mono-specic oak plots (oak-mono) was set to 100% and the
element pools under aspen-oak or birch-oak systems could be smaller or larger
than that, respectively. Test results of pair-wise comparisons of means of empirical
data can be found in Tables S3S6.

oak, while in Sobernheim only those in aspen-oak were signicantly larger than in mono-specic oak stands.
In Kirchberg, the exchangeable pools of Mg were 40 (25), 25
(25) and 14 (6) kg ha1 in aspen-oak, birch-oak and mono-specic
oak plots, respectively; the corresponding pools in Sobernheim
were 26 (6), 20 (5) and 17 (8) kg ha1 in mono-specic oak,
aspen-oak and birch-oak, respectively. Also the Mg pools in
Kirchberg under aspen-oak and birch-oak stands were signicantly
larger than in mono-specic oak, while in Sobernheim only in
aspen-oak stands signicantly larger pools than in mono-specic
oak stands were observed.
The pools of N were 1680 (417), 1613 (266) and 1595
(353) kg ha1 in aspen-oak, birch-oak and mono-specic oak plots
in Kirchberg and 1122 (187), 1171 (158) and 1293 (165) kg ha1 in
aspen-oak, birch-oak and mono-specic oak in Kirchberg. No signicant difference were observed in Kirchberg, but in Sobernheim
the N pools in 010 cm mineral soil under mono-specic oak plots
were signicantly larger than under aspen-oak plots. P pools in
mineral soils were not analyzed.

Fig. 10. Comparison of the amount of biomass (bulk wood including bark with
diameter > 7 cm) that can be harvested per mass unit nutrient element from several
tree species of central Europe. The larger the biomass per unit nutrient the lower
the nutrient cost of biomass harvest. Error bars indicate the standard deviation
among sample trees. Different letters indicate signicant differences between tree
species and were produced from multiple pair-wise comparisons of means. Data
were compiled from this study, Jacobsen et al. (2003) and Pretzsch et al. (2013)
(sample sizes: Betula pendula x Betula pubescens 12, Fagus sylvatica 195, Picea abies
123, Pinus sylvestris 94, Populus tremula x Populus tremuloides 14, Pseudotsuga
menziesii 72, Quercus ssp. 101).

In model (1) the xed study site effect generally explained a signicant share of variation (Table S16) for all elements except Ca, and
soil depth and often the interaction of soil depth  treatment and
soil depth  study site were signicant xed effects, too. According to this model the Ca pools were up to 140%, K up to 56% and
Mg pools up to 165% higher in mineral soils between 0 and 10 cm
depth under aspen-oak or birch-oak plots compared to soils under
mono-specic oak plots (Tables S3 and S4). A similar pattern was
observed in the mineral soil between 10 and 30 cm depth.
3.3. Nutrient element costs of wood
According to model (2) the xed effects tree species and
biomass compartment both signicantly affected the nutrient element costs of the harvestable woody biomass (Table S17). On average 25%, 41%, 39% and 2% less total aboveground woody biomass

66

H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

per unit Ca, K, Mg and P could be harvested from aspen when compared to birch; 9% more aboveground woody biomass could be
harvested per unit N from aspen than from birch. Alternatively,
69%, 47%, 54% and 13% less stem wood and stem bark per unit
Ca, K, Mg and N might be removed from aspen than from birch
and 5% more stem wood and stem bark could be harvested per unit
N from aspen compared to birch. An additional analysis of variance
using our empirical data supported these model predictions, indicating signicant differences in K and Mg costs between aspen
and birch (Fig. 10, Tables S18 and S19).
Considering the harvest of woody biomass compartments with
diameters larger than 7 cm of major tree species in central Europe,
woody biomass of Pseudotsuga menziesii had the lowest Ca costs,
whilst aspen and birch took a moderate rank among most other
species; Ca costs of aspen and birch stems were signicantly lower
than those of Quercus ssp. K costs, on the other hand, were moderately high in birch and Picea abies. In contrast, K costs of aspen and
oak stems were comparatively high and Mg costs were lowest for
stems of Pseudotsuga menziesii. In general, N and P costs of aspen
and birch woody biomass were comparatively high.
Finally, harvesting without branches increased the amount of
woody biomass per unit Ca, K, Mg, N and P in aspen by 12%, 11%,
17%, 30% and 44% and in birch by 23%, 39%, 32%, 35% and 63% irrespective of the study site (Eq. (2)).

4. Discussion
4.1. Effects of nurse crops on productivity
Many trials have studied the effect of tree species mixtures on
stand productivity compared to pure plantations (Man and
Lieffers, 1999; Binkley, 2003; Forrester, 2014). Only few studies
have focused on tree species mixtures with aspen or birch (Man
and Lieffers, 1999; Bergqvist, 1999; Johansson, 2003; Comeau
et al., 2009). We are not aware of studies that have considered
aspen and birch as nurse crops with rotations of only two decades.
In this study, aspen and birch at 4  4 m plant spacing in aspenoak and birch-oak plots produced between 59 and 96 Mg of aboveground woody biomass per ha. This biomass was harvestable after
20 years (or earlier) and corresponded to a mean annual increment
between 3 to 5 Mg ha1 year1 (Fig. 2, Tables S1 and S2). Despite
the water logged soil conditions and the cool mountainous climate,
the productivity of the studied nurse crops were comparable to
that of other widely spaced nurse crops in Germany (Nelson
et al., 2012; Unseld et al., 2012). They were also comparable to productivities reported in the literature for some aspen or birch shelter woods in Estonia or Sweden (Maard, 1996; Bergqvist, 1999;
Johansson, 2003; Karacic et al., 2003), but signicantly lower,
approximately only 50%, than the productivity reported for plantations in Denmark and Germany (Nielsen et al., 2014; Liesebach
et al., 1999). However, the difference may be explained by the
much lower stocking of the studied nurse crops and also the lower
fertility of forest soils when compared to former agricultural soils
that are typically used for woody biomass plantations.
Despite of their comparatively slow growth, mono-specic oak
stands had produced as much biomass at the age of 20 years as
aspen or birch nurse crops. This may be mostly attributable to their
much higher stand densities of approximately 5000 N/ha. Additionally, it may also be related to the contrasting, species-specic
growth dynamics of aspen, birch and oak. During the rst decade
post establishment, high biomass growth in aspen and birch stands
would have exceeded those in mono-specic oak stands, but also
peaked early to subsequently decline below the level of monospecic oak stands leading to comparable biomass pools at the
age of 20 years (Gutsell and Johnson, 2002).

In contrast, oaks growing in the understorey of aspen-oak or


birch-oak plots produced only 35% of the biomass in mono-specic oak stands. Nevertheless, these oaks planted under nurse
crops were ve years younger than aspen, birch and mono-specic
oak stands and also had much lower stand densities compared to
the mono-specic oak stands. Also, between 2006 and 2011, the
understorey oaks suffered from the strong competition by the
aspen and birch overstorey (Ammer and Dingel, 1996). Yet, based
on other studies (Utschig and Pretzsch, 2001) one can expect that
the understorey oaks will respond with increased growth once the
aspen and birch canopy is removed.
However, contrary to our initial assumptions, the total production of harvestable biomass in aspen-oak or birch-oak stands in
this study was not higher than in conventional, mono-specic
oak stands (Table 1 and Fig. 4). Thus, the studied nurse crop systems can be regarded as sub-optimal with respect to oak as the
understorey target tree species and also with respect to its spatial
arrangement (Unseld et al., 2012). If oaks were to be used as the
target tree species in nurse crop systems, then their establishment
in clusters in gaps between widely spaced nurse trees would
reduce the competition for light and thereby also increase their
vitality and productivity (von Lpke, 1998; Saha et al., 2013;
Forrester, 2014). Generally, nurse crop systems are likely more successful if a pronounced complementarity in light use through canopy stratication and phenological differences through use of more
shade tolerant, evergreen understorey species such as Abies alba or
Picea abies were used (Lieffers et al., 1996).
Transgressive over-yielding was observed in several studies
that measured productivity in forests with aspen or birch growing
over shade tolerant target species in North America and Scandinavia (Maard, 1996; Bergqvist, 1999; Man and Lieffers, 1999;
Johansson, 2003; Kabzems et al., 2007). This strengthens our initial
assumption that given that a more shade-tolerant understorey
species than Quercus robur or Quercus petraea was used temporary nurse crops could yield additional, harvestable biomass both
in the short and long term when compared to reforestation with
target species only.
Nevertheless, in this study, aspen or birch nurse crops increased
the early production and supply of harvestable biomass by
5996 Mg ha1, which could be used for example for energy purposes after 20 years or even earlier. Forest restoration with nurse
crops of fast growing pioneers may therefore be an important tool
to maintain or increase the mitigation potential of forests at times
when they are disturbed at increasing frequency and intensity
(Schelhaas et al., 2003; Wiesenthal et al., 2006; Osterburg et al.,
2013). Additionally, nurse crops may be an alternative source of
fuel wood or other wood products from abandoned agricultural
lands or from areas where mono-specic coniferous forests shall
be converted into more tree species diverse, uneven-aged systems
(Pommerening and Murphy, 2004; Uri et al., 2007; Unseld et al.,
2012).

4.2. Effects of nurse crops on nutrient cycling


Poor forest soils may be especially negatively affected by disturbance or intensive biomass removal in terms of soil fertility and
ecosystem functioning (Ballard, 2000). Silvicultural methods that
can benet soil fertility are therefore advantageous (Sverdrup
et al., 2006). In our study, we measured signicantly larger pools
of exchangeable base cations in surface mineral soil to 30 cm in
aspen and birch nurse crop plots than in mono-specic oak plots
established without nurse crop (Fig. 9, Tables S3S6). In the context of forest restoration, these results clearly point to a benecial
effect of aspen and birch nurse crops on soil fertility, which may
last well beyond the removal of the nurse crop shelter.

H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

67

There may be three processes responsible for the higher fertility


in the top soil of nurse crop stands (Alban, 1982; Binkley and
Giardina, 1998): 1. reduced leaching of nutrients, 2. increased
uptake and recycling of nutrients, also from deeper soil layers,
and 3. changes in the quality of organic matter.
During the initial phase of stand development our estimates
indicated that statistically signicant differences for aboveground
woody biomass occurred between aspen and birch in nurse crops
on the one side and mono-specic oak plots on the other side only
for the period between 10 and 20 years (Fig. 3), which would suggest that the nutrient sequestration effect of pioneer trees occurred
too late. However, the biomass of grass, leaves and roots in aspenoak and birch-oak plots might have exceeded those in mono-specic oak plots much earlier because of their wide tree spacing
and reduced competition for light (Comeau et al., 2006).
Also, widely spaced pioneer trees likely invested more C into
root growth than oaks (Litton et al., 2007; Poorter et al., 2012;
Stark et al., 2013) thus exploiting larger and deeper layers of soil
using a highly ramied system of ne and small roots (Fig. S3)
(Strong and Roi, 1983; Gale and Grigal, 1987; Bauhus and
Messier, 1999; Rothe and Binkley, 2001). Once base cations were
taken up from soils, aspen trees conserved large quantities of these
in woody tissues and thus prevented them from leaching (Fig. 2,
Tables S3 and S4) (Hendrickson et al., 1987; Man and Lieffers,
1999).
The recycling of Ca and Mg in leaf litter gained in importance
with stand development (Fig. 5, Tables S13 and S14) (Van Cleve
et al., 1983; Pastor et al., 1984; Par and Cleve, 1993; Alriksson
and Eriksson, 1998). Nurse crops and especially aspen thereby
measurably increased base cation saturation (Fig. 7, Tables S13
and S14) and pH (Fig. 6) in the surface mineral soil when compared
to mono-specic oak plots. In addition, aspen and birch nurse crops
may have increased the abundance of earth worms (Saetre et al.,
1999; Reich et al., 2005) and thus the incorporation of organic matter into mineral soils, providing additional exchange sites
(Alriksson and Eriksson, 1998) charged with a higher proportion
of base cations. However, abundance of earthworms and other soil
fauna was not measured in our study.
Moreover, the organic matter derived from aspen and birch leaf
and root litter appeared to have a higher exchange capacity than
organic matter derived from oaks independent of pH (Fig. 8).
All these processes inuenced the cycling and re-distribution of
nutrients leading to higher nutrient element stocks in surface mineral soils under aspen and birch, when compared to pure oak plots
(Tables S3 and S4) (Bocock and Gilbert, 1957; Harrison, 1971; Man
and Lieffers, 1999).
However, depending on the future development of the different
stand types, the re-distribution of nutrients within the ecosystem
may change upon nurse crop removal. Also, the removal of nurse
crop biomass from aspen-oak and birch-oak plots (Fig. 2), when
compared to mono-specic oak plots, reduces the ecosystem nutrient pools (Fig. 9 and Tables S3S6). Therefore, any reductions in the
nutrient costs of biomass removals, such as using nutrient-efcient
tree species, will also increase the benets of nurse crop systems
on soil fertility (Hendrickson et al., 1987; Ranger and Turpault,
1999).

species for N and P. When compared to the nutrient element costs


for wood of several other major tree species of economic importance in central Europe, nutrient element costs of birch wood were
mostly lower, whereas nutrient element costs for aspen wood were
often higher (Pastor et al., 1984; Par and Cleve, 1993).
However, in addition to the nutrient costs of wood, the nutrient
accumulation and retention potential of species in the ecosystem
should be considered. The high concentrations of base cations in
aspen biomass tissues such as branches, stem wood and stem bark
(Tables S7 and S8) contributed substantially to the observed high
accumulation of nutrient elements in top mineral soils (Figs. 5
and 9, Tables S3S6) and thus its nutrient accumulation and retention potential (Pastor et al., 1984). In nutrient rich systems, where
leaching following disturbance may take on larger dimensions as
the nutrient loss with removal of biomass (Johnson and Todd,
1987), species such as aspen with woody tissues rich in nutrient
elements may provide the greatest benets. In nutrient poor systems, where the nutrient loss with removal of biomass may be
higher than a potential loss via leaching (Hornbeck et al., 1986),
species such as birch with low nutrient element costs of biomass
harvest, may be the more suitable option.
Finally, reducing the harvesting intensity from total aboveground woody biomass to stem only harvest (stem wood and bark)
would additionally reduce the nutrient element costs of biomass
harvest (Tables S18 and S19) (Freedman et al., 1986; Meiwes,
2010; Weis and Gttlein, 2012; Merino et al., 2005). Because of
the species-specic biomass compartmentalization and nutrient
element concentrations (Jacobsen et al., 2003; Rademacher,
2005; Andr et al., 2010) the on-site retention of branch biomass
achieved a higher reduction of nutrient element costs in birch than
in aspen trees.
Thus, depending on the site-specic management targets, the
selection of tree species and the harvest intensity strongly inuence the amount of nutrients that is removed during harvesting
operations and its effects on ecosystem nutrient cycling.

4.3. Nutrient element costs of wood

Funding was provided by the Energy Research Foundation (SEf),


the Ministry of Science, Research and the Arts of the German federal state of Baden-Wrttemberg as well as the Research Institute
for Forest Ecology and Forestry of the German federal state of
Rhineland-Palatinate (FAWF). We would like to thank David
Forrester, Partap Khanna, Merle Koelbing, Bruntje Ldtke, Renate
Nitschke, Matthias Schmidt, Volker & Kerstin Stark, Tim Steinkraus,
Luise Stephani, Julius Schuck, Gebhard Schler, Rdiger Unseld and
Klaus v. Wilpert for their kind support and advice. The constructive

Nutrient costs of biomass removal can vary greatly between


tree species. The selection of species with comparably low nutrient
costs may be crucial to ensure nutrient sustainability (Wang et al.,
1991; Sverdrup et al., 2006; Par et al., 2013). In our study the
mean Ca, K, and Mg costs of birch stem wood and stem bark were
only 69%, 47% and 54% Mg of that of aspen (Fig. 10, Tables S18 and
S19), while there was a much smaller difference between these

4.4. General conclusions


In contrast to many other regions, conventional forest management in central Europe has paid little attention to pioneer trees
such as aspen and birch. With frequent forest disturbances and
increased demand for woody biomass (Gardinier et al., 2013), pioneer trees such as aspen and birch may gain more prominence in
forest management in central Europe and beyond. In addition to
protecting seedlings of target tree species against environmental
extremes (Keenan et al., 1995; Schmidt-Schtz and Huss, 1998),
nurse crops of aspen or birch can benet forest biomass production
and soil fertility. Overall benets may increase when aspen and
birch are established as mixed-species nurse crops with shadetolerant target tree species. Given a proper management (Unseld
et al., 2012), such nurse crop systems may therefore be a suitable
tool to increase productivity and short-term biomass supply in
large forest openings, abandoned agricultural lands or degraded
forest sites.
Acknowledgments

68

H. Stark et al. / Forest Ecology and Management 339 (2015) 5770

and detailed comments of the anonymous reviewers helped much


to improve the quality of the manuscript.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.foreco.2014.1
2.003.
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