Drivers of carbon sequestration by biomass compartment of riparian forests [original]

Drivers of carbon sequestration

by biomass compartment of riparian forests

I. RIEGER,

1,2,3,

I. KOWARIK,

1,2

AND A. CIERJACKS

1,2,3

Technische Universita¨t Berlin, Department of Ecology, Ecosystem Science/Plant Ecology, Rothenburgstraße 12, 12165 Berlin, Germany

Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), 14195 Berlin, Germany

Universita¨t Hamburg, Biocenter Klein Flottbek, Biodiversity of Useful Plants, Ohnhorststraße 18, 22609 Hamburg, Germany

Citation: Rieger, I., I. Kowarik, and A. Cierjacks. 2015. Drivers of carbon sequestration by biomass compartment of

riparian forests. Ecosphere 6(10):185. http://dx.doi.org/10.1890/ES14-00330.1

Abstract. Riparian forests are expected to play a crucial role in the global carbon (C) cycle but the

complex mechanisms of C sequestration in forests remain poorly understood. This study used a

comprehensive approach to analyze C sequestration that included the main C compartments in forests, i.e.,

litterfall, fine roots, and aboveground woody biomass. We aimed at modeling each of them in response to

an array of environmental drivers to untangle the functioning of C sequestration by compartment. The

study was conducted in a Central European riparian forest that is part of the Donau-Auen National Park in

Austria. Carbon sequestration by compartment was correlated with environmental parameters (climate,

stream flow, hydrological, spatial, and forest stand parameters) using generalized linear mixed models

(GLMM), and the correlations were prioritized by hierarchical partitioning. Our results suggest divergent

responses of C sequestration in different ecosystem compartments under dry and wet soil conditions. In

particular, dry conditions led to significantly higher C sequestration in aboveground woody biomass

(larger distance to the low groundwater table), whereas wetter conditions fostered C sequestration in fine-

root (smaller magnitude of fluctuation in the groundwater table) and leaf biomass (smaller distance to the

low groundwater table). Fine roots and litterfall responded to short-term variations in climate (mean

annual temperature) and flooding parameters (duration of the low to mean Danube River water level in the

previous dormant season), highlighting the pivotal role of the dynamic fine-root and leaf biomass

compartments for C uptake in forest ecosystems. Consequently, litterfall and fine roots should be

considered to improve the sensitivity of C sequestration model responses to climate scenarios.

Key words: climate; Danube River; fine roots; flooding; Fraxinus excelsior; generalized linear mixed model; hydrology;

litterfall; Populus alba;Quercus robur;Salix alba; stem production.

Received 16 September 2014; revised 26 March 2015; accepted 13 April 2015; published 22 October 2015. Corresponding

Editor: Y. Pan.

Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the

original author and source are credited. http://creativecommons.org/licenses/by/3.0/

E-mail: [email protected]e

INTRODUCTION

Carbon dioxide release from deforestation is

the second largest source of human-induced

global greenhouse gas emissions, accounting for

about 17%(IPCC 2007). The potential loss of

organic carbon (C) from deforestation can be

estimated by the determination of C stocks in

forests (e.g., Pan et al. 2011, Baccini et al. 2012,

Houghton et al. 2012). Many studies on C stocks

have focused on large forest biomes at the

continental scale. Pan et al. (2011) reported, for

example, that approximately 471, 272, and 119 Pg

C of the world’s forests C stock are stored in

tropical, boreal, and temperate forest ecosystems,

with the contribution of the aboveground bio-

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mass in comparison to soil C stock increasing in

importance from boreal to tropical forests.

Identifying factors that drive C sequestration

in forests is crucial for a mechanistic understand-

ing of this ecosystem process that is increasingly

understood as a critical ecosystem service in the

face of the changing climate. Actual C stocks in

forests are known to depend on an array of

parameters such as forest age (Pregitzer and

Euskirchen 2004), length of growing season,

mean temperature, and precipitation or radiation

balance (Reich and Bolstad 2001), along with

forest fires, harvesting, herbivory, and climate

change (Gloor et al. 2009, Pan et al. 2011,

Sieva¨nen et al. 2014). However, many approach-

es often fail to provide insights into the mecha-

nisms of C sequestration which function at the

local ecosystem scale and ultimately determine

forest C stocks.

Analyzing C sequestration in different biomass

compartments is a promising approach to un-

derstand the formation of C stocks. In contrast to

C storage, which reflects the net outcome of

carbon changes from different ecosystem com-

partments (Fahey et al. 2010), annual C seques-

tration immediately responds to changing

climate and site-specific environmental parame-

ters. This is particularly true for fine roots, which

are the most dynamic compartment and repre-

sent a significant part of net primary production

(NPP; Megonigal and Day 1992, Gordon and

Jackson 2000). A similarly dynamic behavior may

also be assumed for leaves, e.g., in terms of leaf-

out times of temperate forests (Polgar and

Primack 2011) along with variable periods of

photosynthesis.

Riparian forests at the transition zone between

aquatic and terrestrial forest ecosystems offer the

unique opportunity to reveal mechanisms of

biomass C sequestration along varying environ-

mental gradients and for different key tree

species. As a consequence of periodic flooding

and associated geomorphological processes, nat-

ural riparian forests are characterized by a

complex and shifting mosaic of forest patches

that reflect the highly dynamic aspects of

environmental gradients (Naiman and De´camps

1997). The myriad resulting microsites—and

their variance across time and space (Gurnell

2014)—modify species biomass productivity,

diversity and density within these ecosystems

(Mitsch and Gosselink 1993).

Owing to continuous water and nutrient

supply, temperate moist (riparian) forests are

among the most productive forest ecosystems

(Naiman and De´camps 1997, Kiley and Schneider

2005, Keith et al. 2009). Overbank and below-

ground flooding in many cases increases above-

ground NPP (Burke et al. 1999, Dufour and

Pie´gay 2008), litter production (Conner and Day

1992), and fine-root stocks and productivity

(Williams and Cooper 2005, Rieger et al. 2013).

At the same time, frequent and long-term

flooding along with water saturation in the soil

may also lead to reduced aboveground NPP

(Megonigal et al. 1997, Rieger et al. 2013) and fine

root amount and production (Day et al. 1988,

Day and Megonigal 1993, Baker et al. 2001, Kiley

and Schneider 2005). The resulting C sequestra-

tion patterns may be further modified by

sedimentation rates (Cavalcanti and Lockaby

2005), the flooding tolerance of tree species

(Burke and Chambers 2003, Predick et al. 2009),

tree species richness (Giese et al. 2000), forest

stand parameters (Giese et al. 2003, Meier et al.

2006, Cierjacks et al. 2011) and by the seasonality

of flooding (see Day et al. 1988 for aboveground

production; Day et al. 1988 and Burke and

Chambers 2003 for fine-root production).

The trade-offs in C compartments have been

the focus of other studies comparing, e.g., above-

and belowground biomass stocks (Day and

Megonigal 1993, Giese et al. 2003, Rieger et al.

2013), woody and litter biomass production

(Megonigal et al. 1997, Burke et al. 1999), or root

and shoot growth (Day et al. 1988, Megonigal

and Day 1992). Increased winter and spring

flooding, for example, may result in higher

aboveground production but in decreased be-

lowground production (Day et al. 1988). These

results have been supported by some studies

(Megonigal and Day 1992, Day and Megonigal

1993), but—for the same study area—different

results for aboveground NPP in relation to soil

moisture have also been reported (Day et al.

1988, Megonigal et al. 1997). In addition, C

sequestration in moist forests equally depends on

the interaction of site-related environmental

gradients as well as climatic and flooding

variables. In this context Dufour and Pie´gay

(2008) could not find any influence of climate and

stream flow time series on tree-ring growth,

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RIEGER ET AL.

whereas e.g., Kiley and Schneider (2005) attri-

buted differences in annual root biomass to

varying precipitation. Moreover, the influence

of the above-mentioned environmental parame-

ters presumably varies by tree species (Lambers

and Poorter 1992).

To our knowledge, no study has yet addressed

the manifold drivers of biomass C sequestration

in different ecosystem compartments in riparian

forests. As a consequence of studying a maxi-

mum of two C sequestration compartments and

their responses to either site-, climate- or flood-

ing-related variables by comparison of different

study sites, the functioning of environmental

drivers of C sequestration in moist forests still

remains uncertain. In addition, most of the

mentioned studies on C sequestration were

carried out in forest swamps. Gonza´lez et al.

(2010a) performed one of the few studies in

riparian forests, and modeled one biomass

compartment (litterfall production) in response

to forest structure, soil, and spatial parameters.

The study raised the question of whether the

environmental factors that influence litterfall

production have the same effects on the NPP of

other compartments.

Following Gonza´lez et al. (2010a), we modeled

C sequestration by biomass compartment and

key tree species in response to climatic and site-

related environmental variables in the riparian

forest of the Donau-Auen National Park in

Austria. With this comprehensive approach, we

hope to untangle the complex mechanism of C

sequestration in biomass.

Fine roots and leaves directly interact with

their environment (Eisenstat and Caldwell 1988,

Baker et al. 2001, Liu et al. 2004) to ensure the

supply of nutrients for photosynthesis, whereas

aboveground woody biomass fulfills a reserve

function (Pallardy and Kozlowski 2008). Fine

roots and litterfall are also sensitive indicators of

environmental changes (Vogt et al. 1993, 1996)

and are likely to be more responsive parts of NPP

than aboveground biomass. We therefore hy-

pothesized that (1) climatic and stream flow

parameters are more relevant for predicting C

sequestration in the fine-root and litterfall com-

partmentsthanintheabovegroundwoody

biomass compartment, which may be expected

to buffer short-term environmental changes, and

(2) fine roots and litterfall respond similarly to

environmental changes.

In particular, our study aims at (1) quantifying

C sequestration in litterfall, fine-root and above-

ground woody biomass of key tree species in a

temperate riparian forest ecosystem and (2)

modeling C sequestration in the different bio-

mass compartments in response to environmen-

tal gradients (climate, stream flow, spatial,

hydrological, and tree parameters) using gener-

alized linear mixed models (GLMM).

METHODS

Study area and study design

Our study was performed in the Donau-Auen

National Park in Austria, in the floodplains east

of Vienna. Since 1997, the national park has been

recognized as Category II of the IUCN (Interna-

tional Union for Conservation of Nature and

Natural Resources). It preserves one of the largest

remaining near-natural riparian forests in Central

Europe. About 65%(6045 hectares) of the

national park is covered by riparian forest

(Donau-Auen National Park 2014a); the remain-

der comprises mostly meadows and water

courses. Climatic conditions for the period

1948–2008 were characterized by a mean annual

temperature of 9.88C and mean annual precipi-

tation of 533 mm (climate station: Schwechat

48870N, 168340E, 184 m above sea level;

Zentralanstalt fu¨ r Meteorologie und Geodyna-

mik 2002).

In the studied river section, the main channel

of the Danube River is approximately 350 m in

width and drains an area of 104,000 km

. The

banks are predominantly fixed by riprap. In

addition, a part of the area is diked. However, the

Danube River still inundates large areas during

high river water levels. The magnitude of

fluctuation of the Danube River water level is

up to 7 m and water discharge is mainly

mediated by snowmelt in the Alps and by heavy

rainfalls in the upstream watershed causing

overbank flooding mainly in summer (Donau-

Auen National Park 2014b). The slope of the river

is 0.043%with low and mean annual discharges

of 900 and 1,950 m

1

, respectively. The mean

annual flood discharge is 5,270 m

1

(Tockner et

al. 1998).

The riparian forest is composed of different

vegetation units with specific tree-species com-

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RIEGER ET AL.

position (Drescher and Fraissl 2006, Cierjacks et

al. 2010). Cottonwoods dominated by Populus

alba, P. nigra, and Salix alba prevail at sites

characterized by a high frequency of overbank

flooding and high flow velocities close to the

main channel and side channels as well as at sites

with a high groundwater table as in historic river

beds. At less dynamic sites with a lower

inundation frequency, Ulmus laevis initiates the

formation of hardwood forests, which contain

overstory tree species such as Quercus robur and

Fraxinus excelsior (Drescher and Fraissl 2006).

Forest structure and species composition are

comparable on both sides of the dike (pers.

observation). Forestry activities have been

banned since the establishment of the National

Park in 1996 (Austria’s Federal Law; Art. 15a, B-

VG), but areas of natural forest still alternate with

older plantings of Populus 3canadensis or

monoculture sites where P. alba has regrown

after clear cutting (Drescher and Fraissl 2006).

Soil types are also very heterogeneous varying

from rambla to eutric calcaric fluvisols and haplic

calcaric gleysols (Cierjacks et al. 2010).

The study area comprised the riparian forest to

the north of the Danube River. The villages

Scho¨nau in the west (48880N, 168360E, river

kilometer 1910) and Stopfenreuth downstream to

the east marked the beginning and end, respec-

tively, of the study area (Fig. 1). To cover the

entire spatial variability of the hydrosystem

(Pie´gay and Schumm 2009) and a broad range

of environmental gradients, the study area was

divided into three lateral and two longitudinal

zones. In two lateral zones (400 m and .400 m

to the Danube River), overbank flooding is still

present, whereas in the area north of the dike,

surface flooding is inhibited. Two longitudinal

zones divide the lateral zones into an upstream

and a downstream part of the study area. Within

each of the resulting six zones, we randomly

selected two—sociologically dominant—sample

trees 25 cm diameter at breast height (DBH) out

of the four main tree species using the national

park’s forest inventory database (100 3400 m

grid). The tree species Q. robur and F. excelsior

were chosen as representatives of hardwood

forest; P. alba and S. alba are typical species of

cottonwood forests. Overall, 48 sample trees

were included in this study (6 zones 32

individuals 34 tree species ¼48 sample trees).

Site-related environmental parameters were mea-

sured once between January and June 2010.

Carbon sequestration in litterfall

Beneath the canopy of each sample tree, one

litter trap (0.5 31 m) was randomly placed at an

elevation of one meter above the ground. Due to

the fact that we considered all relevant tree

species of the study area, we assume litterfall

values to be representative for the studied

riparian forest. Litterfall traps were installed in

April 2010 and remained in the forest until

March 2013. Annual litter samples (2010, 2011,

and 2012) were collected in the last week of

November. Each trap was post-controlled in

February of the following year to collect late

litterfall, which was most notable in S. alba

sample trees. Leaves, woody material, and

generative tissues of Q. robur and F. excelsior

were analyzed separately. Samples were dried at

658C in a ventilated oven to a constant mass.

Biomass was weighed and doubled to calculate

the annual litterfall production per m

. Biomass

was then multiplied by 0.475 to derive the C

amount in the leaves, woody material, and

generative tissues (Magnussen and Reed 2004,

Gonza´lez 2012).

Carbon sequestration in fine roots

Annual fine-root productivity was estimated

using ingrowth cores. We placed two ingrowth

cores 50 cm apart in November 2010. Both cores

were buried 2 m from the sample tree to avoid

the effects of local sedimentation caused by the

trunk. Ingrowth cores were cylindrical (3.5 cm in

diameter and 30 cm in length) and made of

fiberglass fabric of 1.2 mm mesh size and a

fishing line (0.15 mm, Berkley Fireline, Columbia,

South Carolina, USA) sewn with a sewing

machine (Singer 354, Singer, New York, New

York, USA). The position of each core was

recorded and labeled with a plastic card at the

end of a ca. 20 cm long nylon thread to facilitate

retrieval after sediment deposition. To ensure

relative comparability between different sites, all

cores were filled with the same root-free silty to

sandy sediment that is typically deposited by the

Danube River during surface flooding. Sediment

was directly taken from the shore of the Danube

River.Thefirstcorepersampletreewas

harvested after one year, the second after two

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RIEGER ET AL.

years. In total, we were able to harvest 46 intact

ingrowth cores in November 2011 and 45 cores in

November 2012. Fine roots of each ingrowth core

were washed, using a series of sieves of different

mesh sizes (2.5 mm on the top, 0.5 and 0.2 mm in

the middle, and 0.063 mm at the bottom), and

then stored at 48C in a refrigerator. They were

then separated by size and phenology classes

(usually within 24 hours). For classification, fine

roots were homogenously distributed in a petri

dish which was lined with millimeter paper. Six

of twenty marked square centimeters were

randomly chosen as a sub sample to classify fine

roots according to their diameter size (,0.49, 0.5–

1.49, 1.5–2.99, and 3–5 mm) and into living and

dead fine roots using a stereo microscope (Leica

Wild M3C, Leica, Wetzlar, Germany). Living fine

roots and necromass were separated according to

Persson (1980a,b) and McClaugherty et al. (1982).

Fine root samples were dried to constant weight

and weighed. Carbon amount was calculated by

multiplying biomass values by 0.5. Fine-root

growth rates for 2012 were calculated as the

difference between biomass measured in 2012

and in 2011.

Carbon sequestration of aboveground woody

biomass

At each sample tree, a permanent measuring

tape (Permanent D) was fixed at breast height to

determine the annual growth in DBH. From

February 2010 to February 2013, DBH was

recorded every two months. Based on DBH and

height of the sample tree, we used allometric

equations (Table 1; Zianis et al. 2005) to calculate

the total aboveground biomass in 2010, 2011, and

2012. Increment of aboveground biomass was

calculated as the difference in biomass stocks

between two consecutive years. Aboveground

biomass equations were not available for S. alba,

so stem volume equations were used for this

species and were transformed to biomass using

the factor 0.5321 according to Lehtonen et al.

(2004). Carbon stocks were derived from biomass

values as described for litterfall. One Q. robur

sample tree was excluded because the measuring

tape was stolen.

Due to the heterogeneity of the studied

riparian forest surrounding the sample tree,

e.g., forest stock, basal area, age of different tree

species, coverage etc., we decided to present tree-

based values for C sequestration in aboveground

woody biomass instead of extrapolated hectare

values with great uncertainties.

Spatial and hydrological parameters

The spatial position of each sample tree was

recorded before foliation in 2010 to a precision of

approximately 10 cm with the help of a differen-

tial GPS (Trimble GeoXH 2005 series handheld,

Fig. 1. Study area within the Donau-Auen National Park in Austria and study design.

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RIEGER ET AL.

Trimble, Sunnyvale, California, USA). For each

sample tree, we determined the following spatial

parameters: the lateral distances to the Danube

River and to the nearest side channel, the vertical

distance to the mean Danube River water level,

and the longitudinal distance, which is the

distance to the upstream beginning of the study

area to the west near the village Scho¨nau (Fig. 1).

Our hydrological parameters were based on a

groundwater model provided by the Technical

University of Vienna. We calculated the distance

to the groundwater table at its lowest level and

the magnitude of fluctuation of the groundwater

table between its low and mean levels (see Rieger

et al. 2013, 2014 for more details).

Climatic and stream flow parameters

As no meteorological data for 2012 were

available for the nearest climate station (Schwe-

chat), mean monthly and annual climatic param-

eters (temperature, precipitation) for 2009–2012

were derived from the meteorological station of

Vienna–Hohe Warte, located at about 23 km

westwards from the upstream beginning of the

study area (488250N, 168360E, 209 m asl;

Zentralanstalt fu¨ r Meteorologie und Geodyna-

mik 2013).

Daily river water levels for the period 2009–

2012 were provided by via donau–O

¨sterreichi-

sche Wasserstraßen-Gesellschaft mbH for the

water-gage monitoring station Wildungsmauer

(Danube River kilometer 1894.72; 4880605700 N,

1684802500 E). Flooding parameters were calculat-

ed for each year, with the same value for all

sample trees, as total days per growing season

(April–September) and dormant season (Octo-

ber–March) in which the Danube fell below,

ranged between, or exceeded long-term average

water levels defined by via donau–O

¨sterreichi-

sche Wasserstraßen-Gesellschaft mbH (2012; Ta-

ble 2). We used the number of days with Danube

River water levels below RNW (water level

duration exceeding ca. 343 days/year), between

RNW and MW (averaged water level), between

MW and HSW (water level duration exceeding

ca. 3.6 days/year), or above HSW (abbreviations

according to Table 2). Our study includes two

periods with overbank flooding in June 2010 and

January 2011.

Statistics

The whole data set of continuous variables was

analyzed in terms of homogeneity (Fligner test),

normality (Shapiro-Wilk test), outliers or missing

values (Zuur et al. 2010). Generalized linear

mixed models (GLMM) were chosen to deter-

mine which environmental gradients were influ-

ential in determining C sequestration in litterfall,

fine roots and aboveground woody biomass

since our data set is based on repeated measure-

ments over three consecutive years on the same

sample trees, which causes temporal autocorre-

lation (Crawley 2007, Zuur et al. 2009). Spatial,

hydrological and climatic variables were defined

as fixed effects, whereas sample tree and time

were defined as random effects. Owing to

negative values in the Poisson family, which are

not allowed in the calculation, we transformed

three negative values of the data set to zero to

meet the requirements of modeling C sequestra-

tion in aboveground woody biomass and fine

roots, respectively. Verification of the final

model’s variable selection was done using both

stepwise forward and backward selection of

predictor variables. To facilitate model selection

based on minimum AIC values, we used the lmer

Table 1. Allometric equations by tree species used for biomass calculations in the study area (Abbreviations: AB¼

aboveground biomass, ABW ¼aboveground woody biomass, SV ¼stem volume, D¼diameter at breast height,

H¼height, App. ¼Appendix).

Species Equation

Units Equations used from

Zianis et al. (2005)AB ABW SV D H

Quercus robur ln(AB) ¼(0.883) þ(2.14 3ln(D)) kg cm App. A, #600

Fraxinus excelsior ln(ABW) ¼2.4598 þ2.4882 3ln(D) kg cm App. A, #134

Populus alba AB ¼0.0519 3D

2.545

kg cm App. A, #514

Salix alba SV ¼1.8683 þ0.2146 3D

þ0.0128

þ0.0138 3H

3D

0.0631 3H

cm m App. C, #218

Equation for Salix caprea was used.

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RIEGER ET AL.

function of the lme4 package. The calculated

models include spatial (e.g., vertical, lateral and

longitudinal gradients) and hydrological (e.g.,

magnitude of fluctuation in the groundwater

table, distance to low groundwater table) vari-

ables, tree species and annual climatic and

flooding parameters. The relative contributions

of all significant variables in the final models to

the explained variance were calculated using the

hier.part function of the gtools package.

All calculations were performed with R ver-

sion 1.19.4.7 using the packages AED, gtools,

hier.part, mass, lme4, and nlme (R Development

Core Team 2011).

RESULTS

Carbon sequestration in biomass compartments

Mean annual C sequestration in aboveground

biomass was 20.6 kg C yr

1

per studied tree,

whereas litterfall and fine roots summed up to

0.5 kg C m

2

1

. Carbon sequestration in

litterfall was 63%greater than in fine roots (Table

3).

The majority of litterfall consisted of leaf

biomass (74%). In fine roots about 95%could

be attributed to living fine-root biomass, and

most was found in the size classes ,0.5 mm

(48%) and 0.5–1.49 mm (30%; Table 4).

Correlation analysis did not reveal significant

interactions among biomass compartments (Pear-

son’s product moment correlation p.0.05)—

regardless whether the mean values for C

sequestration in litterfall, fine roots, and above-

ground woody biomass were considered for the

whole time period or separated by calendar year.

Environmental drivers of carbon sequestration

When the water level of the Danube River

remained below average for longer periods in the

previous dormant season, C sequestration in

litterfall decreased. This was the most meaning-

ful driver of C sequestration in litterfall and

improved significantly the model that based on

spatial, hydrological or tree species as drivers

only (AIC ¼1093.9, p,0.001). Overall, this

stream flow parameter explained 92%of the

variance in the dependent variable (Fig. 2; for

model documentation see Appendix B).

Among all spatial and hydrological drivers

only the distance to the low groundwater table

and tree species remained in the final model of C

sequestration in litterfall (Fig. 2). Carbon seques-

tration in litterfall increased with smaller dis-

tances to the low groundwater table, i.e., trees

produced more litter when the groundwater

remained closer to the surface. When the

interaction between low groundwater level and

tree species was analyzed, it was revealed that C

sequestration of litterfall differed according to the

individual response of each species to the low

groundwater table. In this context, C sequestered

Table 2. Danube River water levels used to describe the flooding intensity of the Danube River (River water levels

according to the reference via donau–O

¨sterreichische Wasserstraßen-Gesellschaft mbH [2012]).

Status Definition

River water level Wildungsmauer

(altitude, m asl)

RNW water level that is exceeded 94%of the year (ca. 343 days) 141.1

MW mean water level 142.41

HSW water level that is exceeded 1%of the year (ca. 3.6 days); corresponds

approximately to the bankful discharge, highest navigable water level

145.12

Table 3. Mean annual C sequestration per study tree (means 6SE) in a riparian forest from 2010 to 2012 (ABW ¼

aboveground woody biomass, litterfall) and from 2011 to 2012 (fine roots, sum) by compartment and separated

into leafs, twigs, and seeds (litterfall) as well as living biomass and necromass (fine roots).

Litterfall compartment

Litterfall

(kg C m

2

1

)

Fine root

phenology classes

Fine root

(kg C m

2

1

)

ABW

(kg C yr

1

)

Leaves 0.23 60.008 Living biomass 0.18 60.031 ...

Twigs 0.08 60.011 Necromass 0.004 60.003 ...

Seeds 0.008 60.003

Total 0.31 60.01 0.19 60.03 20.57 61.67

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RIEGER ET AL.

in litterfall under P. alba was significantly lower

than under F. excelsior,Q. robur, and S. alba (Fig. 2;

for model documentation see Appendix B).

Sequestration of C in fine roots correlated

mainly with the mean annual temperature.

Furthermore, C sequestration in fine roots in-

creased with (1) greater distances to the upstream

boundary of the study area (longitudinal gradi-

ent) and (2) lower magnitudes of fluctuation in

the groundwater table (hydrological gradient).

At 68%, the mean annual temperature explained

the major part of variance, whereas the longitu-

dinal and hydrological gradients accounted

together for only 32%(Fig. 3; for model docu-

mentation see Appendix D). Considering the

annual temperature as a climatic parameter

increased model predictability significantly

(AIC ¼712.0, ANOVA, p,0.001).

The C sequestration of aboveground woody

biomass was significantly influenced by the

distance to the low groundwater table (59%)

and by tree species (37%;Fig.4).Greater

distances to the low groundwater level generally

increased C sequestration in aboveground

woody biomass in all tree species. Furthermore,

C sequestration of aboveground woody biomass

was significantly higher for P. alba compared to S.

alba, whereas F. excelsior and Q. robur occupied an

intermediate position (Fig. 4). Among the climat-

ic parameters neither temperature nor precipita-

tion improved the final model significantly.

However, the duration of the Danube River

water level between the mean and the ten-year

flooding event in the current growing season

significantly improved the spatial model as

demonstrated by a lowered AIC (ANOVA, p,

0.05), which indicates that long-lasting flooding

events significantly reduce C sequestration of the

aboveground woody biomass (for model docu-

mentation see Appendix I).

Table 4. Annual C sequestration in fine roots of a

riparian forest by size class and phenology (means 6

SE) in 2011 and 2012.

Size (mm) and

phenology class

C sequestration (kg C m

2

1

)

2011 2012

,0.50

Living biomass 0.039 60.006 0.144 60.031

Necromass 0.004 60.001 0.002 60.001

0.50–1.49

Living biomass 0.023 60.005 0.091 60.022

Necromass 0.003 60.001 0.000 60.002

1.50–2.99

Living biomass 0.01 60.005 0.025 60.011

Necromass 0.002 60.001 0.001 60.001

3.00–5.00

Living biomass 0.005 60.004 0.030 60.019

Necromass 0.000 60.000 0.000 60.000

Total

Living biomass 0.077 60.011 0.283 60.051

Necromass 0.009 60.002 0.002 60.003

Living biomass

and necromass

0.085 60.011 0.281 60.051

Fig. 2. Generalized linear mixed model for predicting C sequestration in litterfall of riparian forests based on

(A) the Danube river water level, (B) hydrology, and (C) tree species (for model documentation see Appendix B);

values in parentheses refer to the relative influence of each predictor variable to the explained variance.

vwww.esajournals.org 8October 2015 vVolume 6(10) vArticle 185

RIEGER ET AL.

The relative contributions of significant vari-

ables to the explained variance in C sequestra-

tion show that the highly dynamic

compartments of litterfall and fine roots mainly

responded to variable climatic and flooding

parameters (92 and 68%; Figs. 2 and 3). In

contrast, aboveground biomass mainly respond-

ed to more stable environmental gradients such

as the vertical distance to the low groundwater

table and tree species (59 and 37%;Fig.4).

Modeling total C sequestration (combining litter-

fall, fine roots, and aboveground woody bio-

mass) was not satisfactory (for model

documentation see Appendix J).

Fig. 3. Generalized linear mixed model for predicting C sequestration in fine roots of riparian forests based on

(A) the mean annual temperature, (B) spatial, and (C) hydrological variables (for model documentation see

Appendix D); values in parentheses refer to the relative influence of each predictor variable to the explained

variance.

Fig. 4. Generalized linear mixed model for predicting C sequestration in aboveground woody biomass of

riparian forests based on (A) the distance to the low groundwater table, (B) tree species, and (C) the Danube

River water level (for model documentation see Appendix I); values in parentheses refer to the relative influence

of each predictor variable to the explained variance.

vwww.esajournals.org 9October 2015 vVolume 6(10) vArticle 185

RIEGER ET AL.

DISCUSSION

This study provides detailed insights into the

functioning of C sequestration in different

compartments (litter, fine-root and aboveground

woody biomass) of riparian forest ecosystems.

Our results highlight the role of annually

changing climatic and flooding parameters as

the main drivers of C sequestration in fine roots

and litterfall, which makes them more sensitive

indicators for environmental changes than

aboveground woody biomass. Furthermore, lit-

terfall and fine root production proved to

respond similarly to wetter soil conditions. A

positive correlation (Pearson’s product-moment

correlation ¼0.47, p,0.001; data not shown)

between the groundwater-related predictor var-

iables for litterfall (distance to the low ground-

water table) and fine roots (magnitude of

fluctuation in the groundwater table) supports

this assumption. Our study also revealed pro-

nounced differences among biomass compart-

ments and the tree species involved. However,

we could not find a direct correlation between

the studied compartments in terms of C alloca-

tion, which implies a high plasticity within and

among species.

Mean C sequestration in litterfall increased

with a smaller distance to the low groundwater

table, which indicates that wetter soil conditions

in our study area are favorable for litterfall

production. Enhanced litterfall production, e.g.,

owing to increased size or number of leaves, can

be a possible response of plants to optimized soil

water conditions and would reflect increased

photosynthesis rates and carbon dioxide uptake

from the atmosphere (Lu¨ ttge et al. 1999).

Similarly, Poorter et al. (2009) reported a positive

correlation between leaf mass per unit area

(LMA) and soil water saturation. Correspond-

ingly, Brando et al. (2008) found that litterfall

decreased by 23%compared to control after three

years of simulated drought. In contrast, Gonza´lez

(2012) reported a general increase in litterfall

production at greater distances to the ground-

water table and in locations closer to the Middle

Ebro River in Spain. However, these varying

results are not necessarily contradictory as the

distances to the mean groundwater table be-

tween our study and the Ebro River study were

quite different (250 vs. 70 cm, data derived from

Gonza´lez et al. 2010b), suggesting that our study

sites are at the drier end of the spectrum, and the

Ebro study sites were more toward the wetter

end of the ecosystem’secologicalamplitude,

where wetter soil conditions could have been

present. Litterfall productivity increases as the

ecosystem moves towards the optimal hydrolog-

ical regime. In the case of the Danube River these

are rather wet soil conditions, while drier soil

conditions are more favorable in the Middle Ebro

River system. The observations by Gonza´lez

(2012) support this assumption because the

author also attributed decreasing litterfall, in

particular of S. alba and P. alba, to sudden and

long-lasting low-water periods at drier sites.

Similarly to Meier et al. (2006) and Gonza´lez

(2012) who attributed differences in litterfall

productivity to species composition, our results

showed a significant influence of the tree species

on C sequestration in litterfall. Including the

distance to the low groundwater table as an

interaction term in our model showed that

litterfall production of P. alba was significantly

lower compared to S. alba,F. excelsior, and Q.

robur, indicating that P. alba was less tolerant to

lower groundwater tables. Riparian cottonwoods

are known to respond very pronouncedly to

drought stress by reducing stomata aperture and

photosynthesis, which leads to lower growth

rates and canopy dieback (Rood et al. 2003,

Pallardy and Kozlowski 2008). Populus alba is a

fast-growing, water-consuming tree species

which exhibits higher transpiration rates and less

efficient water use compared to genera such as

Fraxinus (Manzanera and Martı´nez-Chaco´n

2007). The significantly lower values of litterfall

in P. alba compared to S. alba seem contradictory

to findings of Gonza´lez et al. (2010c, 2012). Still,

the authors explain this fact by a clearly higher

canopy dieback in S. alba in their study area.

Accordingly, lower values of total and twig

(Kruskal-Wallis test p,0.05; data not shown)

biomass in litterfall along with a higher mean

tree age (data derived from Rieger et al. 2014) in

P. alba compared to S. alba in in the Danube River

floodplain forest point to a similar effect of

canopy dieback on litterfall—albeit here related

to P. alba. Furthermore, S. alba sites tend to be

slightly wetter than P. alba sites (3.3 vs. 3.7 m

distance to the low groundwater table) which

may explain the decreasing C sequestration in

vwww.esajournals.org 10 October 2015 vVolume 6(10) vArticle 185

RIEGER ET AL.

leaves as the depth to the groundwater table

increases (see also Horton et al. 2001). Increased

depths to the groundwater table may be partic-

ularly severe during sunny days at the beginning

of the growing season when bud expansion and

growth of leaves cause maximum water demand.

Wetter soil conditions furthermore increase sol-

uble phosphatases and therefore enhance nutri-

ent availability and uptake (Scheffer et al. 2010),

which may increase litterfall production (Gonza-

lez et al. 2010a).

Theresponseofpresentplantgrowthto

conditions in the previous season is well docu-

mented. The number of leaf primordia and the

leaf area of trees can be lowered by hot and dry

weather in the previous year (Kozlowski 1971).

The results of our study support the assumption

that—in addition to climate—flooding parame-

ters during the dormant season cause changes in

leaf C sequestration. Carbon sequestration in

litterfall responded positively to longer periods

of intermediate Danube River water levels in the

previous dormant season (Fig. 2), which may

indicate conditions that enhance overwintering

of leaf primordia in buds. Our analysis shows

significantly higher values for litterfall in the

years 2011 and 2012 compared to 2010, which

reflects well the number of days of intermediate

water levels during the previous dormant season

of 45 days (2010), 153 days (2011) and 124 days

(2012). The river level is related to other climatic

parameters in the upstream region. Above

average temperatures during the dormant season

in the Alps and Alpine foothills can, for example,

induce earlier snow melt or rainfall and thereby

increase the Danube River to an intermediate

level, possibly leading to higher bud survival and

subsequent leaf development.

Similarly to litterfall, C sequestration in fine

roots was positively correlated to wetter soil

conditions, i.e., the lower the magnitude of

fluctuation between the low and mean ground-

water table, the higher the C sequestration in fine

roots. Carbon stocks of fine roots reflect net

annual C sequestration rates in fine roots.

Consequently, Carbon stocks of fine roots on

the same study plots also increased at greater

distances from the Danube River, where magni-

tudes of fluctuation in the groundwater table are

significantly lower (Rieger et al. 2013). That the

largest portion of living fine-root biomass is

found in the smallest size classes points to a good

nutrient supply and aerated soil conditions—at

least in the top 30 cm—which both reduce fine

root mortality (Rieger et al. 2013) and accelerate

fine root decomposition (Day and Megonigal

1993, Rotkin-Ellman et al. 2004). Moreover at

sites with a low magnitude of fluctuation in the

groundwater table, sedimentation rate is low

(Rieger et al. 2014), which may additionally

increase fine-root growth (Simm and Walling

1998, Cavalcanti and Lockaby 2005); these

conditions are more frequently found at greater

distances to the upstream boundary of the study

area. The re-connection of formerly cut-off side

arms with the main channel of the Danube River

in the upstream region of the study area may

have led to decreased fine root growth due to

increased sedimentation rates.

Carbon sequestration in fine roots also re-

sponded significantly to annually changing

parameters such as mean annual temperature.

Increased mean annual temperatures, particular-

ly at the beginning and the end of the growing

season, can improve fine-root productivity in

temperate zones (Pregitzer et al. 2000) as a result

of better nutrient availability in warmer and

wetter soils due to elevated mineralization rates

(Zak et al. 1999, Davidson and Janssens 2006). In

accordance, Leppa¨lammi-Kujansuu et al. (2014)

linked higher soil temperatures and nutrient-rich

soil with increased below-ground litter produc-

tion (dead fine roots ,1 mm) for Picea abies. The

authors report up to fourfold higher below-

ground litter production for a treatment with

soil warming, fertilization, and irrigation com-

pared to one with irrigation only. Although C

sequestration in aboveground litterfall and fine

roots was not directly correlated in our study, the

same response to wetter soil conditions param-

eters points to a similar C uptake strategy in both

compartments. Under advantageous site condi-

tions (wetter soil), photosynthesis is supported

and linked to an increase in leaf production for

greater C uptake. In parallel, enhanced fine-root

production ensures the supply of additional

water and nutrients.

In contrast to litterfall and fine roots, our

results show that C sequestration in above-

ground woody biomass tended to respond

positively to greater distances to the groundwa-

ter table, i.e., drier soil conditions. This supports

vwww.esajournals.org 11 October 2015 vVolume 6(10) vArticle 185

RIEGER ET AL.

findings on tree C stocks, which also increased

with distance to the groundwater table and

decreased with distance to the main channel

(Rieger et al. 2013). Both results point to a

decrease in stem growth under wet soil condi-

tions with risk of anoxia and water saturation

which presumably forces the trees to allocate

more biomass in fine roots and less in radial

growth. However, our data do not provide final

evidence for a direct negative correlation of fine

root and stem growth and further research is

needed to illuminate this aspect. In addition, C

sequestration in aboveground woody biomass of

riparian forests was also determined by tree

species and was higher in P. alba than in Q. robur

and F. excelsior. This may be attributed to lower

mean tree age in the pioneer species P. alba

(derived from data of Rieger et al. 2013) which

suggests that this species indicates an earlier

succession state with higher C sequestration in

aboveground biomass than climax species such

as Q. robur and F. excelsior. Interestingly, S. alba

had the lowest C sequestration in aboveground

woody biomass despite its character as a fast-

growing pioneer tree. We suppose that diameter

growth in this species is generally lower than that

of P. alba which may explain the significant

differences between both pioneer species.

CONCLUSIONS

In accordance with our first hypothesis, the

relative contribution of all explanatory variables

clearly showed that C sequestration in litterfall

and fine roots was mainly determined by

annually changing environmental variables (i.e.,

duration of the mean water level in the Danube

River during the previous dormant season and

mean annual temperature). These tree biomass

compartments can therefore be considered as the

more responsive in terms of NPP compared to

the aboveground woody part. However, a three-

year study is probably too short to draw

fundamental conclusions on this topic, and we

strongly recommend long-term studies to verify

the results. In contrast, C sequestration in

aboveground woody biomass was predominant-

ly determined by site-specific variables (i.e.,

distance to the low groundwater table) and tree

species. Carbon sequestration in aboveground

woody biomass can be assumed to function as a

nutrient and carbohydrate reservoir that is able

to compensate for the impact of adverse short-

term fluctuations in litterfall and fine root

productivity. It is well known that sequestered

C can fulfill a reserve function, when C is

accumulated in wood and bark tissues (Pallardy

and Kozlowski 2008). However, this pattern

seems to be modified by environmental param-

eters that vary over time, such as temperature or

flooding, and that are related to soil moisture

(distance to and magnitude of fluctuations in the

groundwater table). The latter imply that short-

term C sequestration in litterfall or fine roots is

strengthened if environmental conditions be-

come wetter. Still, both compartments also show

pronounced differences in terms of their response

to particular environmental inputs.

Overbank flooding in our study area seemed to

have a less pronounced influence on C seques-

tration in biomass in comparison to belowground

flooding. Aboveground woody biomass C se-

questration was the only parameter which was

directly influenced by overbank flooding, but the

contribution to the explained variance was very

low, just 2%. In contrast, the groundwater regime

played an important role in the majority of the

models. These findings coincide with the results

on C dynamics from the same study area for C

stocks in biomass (Rieger et al. 2013) and soil

(Rieger et al. 2014), where both C pools also

responded most notably to groundwater. A

rough estimate of hectare-related values of C

sequestration in aboveground woody biomass

(12.98 t C ha

1

based on the stem number per

hectare (Appendix K: Table K1) and C seques-

tration values (Table 3) shows that litterfall and

fine roots account for approximately 23.9%(3.1 t

Cha

1

) and 14.6%(1.9 t C ha

1

) of this amount.

Owing to the suggested contribution of litterfall

and fine roots, and the pronounced spatial and

temporal variability in C sequestration, we

strongly recommend including different ecosys-

tem compartments in C sequestration models to

improve the reliability of predictions of the C

cycle at the ecosystem scale.

ACKNOWLEDGMENTS

This study was funded by the Deutsche Forschungs-

gemeinschaft (DFG, grant number CI 175/1) and was

part of the project ‘‘ Carbon dynamics in soil and

vegetation of riparian forests.’’ We thank Torben Lu¨bbe

vwww.esajournals.org 12 October 2015 vVolume 6(10) vArticle 185

RIEGER ET AL.

and Marius Bednarz for their support during field

stays; our technical assistants Gabriele Hinz and Karin

Grandy for their help in the laboratory as well as

Christian Baumgartner and Christian Fraissl from the

Donau-Auen National Park for their relentless techni-

cal and administrative support over three years of field

campaigns. We also want to thank Kelaine Ravdin for

improving our English and two reviewers for their

helpful comments on an earlier version of the

manuscript.

LITERATURE CITED

Baccini, A. et al. 2012. Estimated carbon dioxide

emissions from tropical deforestation improved

by carbon-density maps. Nature Climate Change

2:182–185.

Baker, T. T., W. H. Conner, G. B. Lockaby, J. A. Stanturf,

and M. K. Burke. 2001. Fine root productivity and

dynamics on a forested floodplain in South

Carolina. Soil Science Society of America Journal

65:545–556.

Brando, P. M., D. C. Nepstad, E. A. Davidson, S. E.

Trumbore, D. Ray, and P. Camargo. 2008. Drought

effects on litterfall, wood production and below-

ground carbon cycling in an Amazon forest: results

of a throughfall reduction experiment. Philosoph-

ical Transactions of the Royal Society B 363:1839–

1848.

Burke, M. K., and J. L. Chambers. 2003. Root dynamics

in bottomland hardwood forests of the Southeast-

ern United States Coastal Plain. Plant and Soil

250:141–153.

Burke, M. K., G. B. Lockaby, and W. H. Conner. 1999.

Aboveground production and nutrient circulation

along a flooding gradient in a South Carolina

Coastal Plain forest. Canadian Journal of Forest

Research 29:1402–1418.

Cavalcanti, G. G., and G. B. Lockaby. 2005. Effects of

sediment deposition on fine root dynamics in

riparian forests. Soil Science Society of America

Journal 69:729–737.

Cierjacks, A., B. Kleinschmit, M. Babinsky, F. Kleins-

chroth, A. Markert, M. Menzel, U. Ziechmann, T.

Schiller, M. Graf, and F. Lang. 2010. Carbon stocks

of soil and vegetation on Danubian floodplains.

Journal of Plant Nutrition and Soil Science

173:644–653.

Cierjacks, A., B. Kleinschmit, I. Kowarik, M. Graf, and

F. Lang. 2011. Organic matter distribution in

floodplains can be predicted using spatial and

vegetation structure data. River Research and

Applications 27:1048–1057.

Conner, W. H., and J. W. Day. 1992. Water level

variability and litterfall production of forested

fresh-water wetlands in Louisiana. American Mid-

land Naturalist 128:237–245.

Crawley, M. J. 2007. The R book. Wiley, Chichester,

UK.

Davidson, E. A., and I. A. Janssens. 2006. Temperature

sensitivity of soil carbon decomposition and

feedbacks to climate change. Nature 440:165–173.

Day, F. P., and P. J. Megonigal. 1993. The relationship

between variable hydroperiod, production alloca-

tion, and belowground organic turnover in forest-

ed wetlands. Wetlands 13:115–121.

Day, P. D., S. K. West, and E. G. Tupacz. 1988. The

influence of ground-water dynamics in a periodi-

cally flooded ecosystem, the Great Dismal Swamp.

Wetlands 8:1–13.

Donau-Auen National Park. 2014a. The National Park:

facts and figures. http://www.donauauen.at/?

area¼nationalpark&subarea¼numbers

Donau-Auen National Park. 2014b. Nature and science:

the Danube. http://www.donauauen.at/?

area¼nature&subarea¼danube

Drescher, A., and C. Fraissl. 2006. Dealpine und

demontane Auen im su¨do¨stlichen Mitteleuropa.

Struktur und Standortsbedingungen von Auenwa¨l-

dern des o¨stlichen Mitteleuropa am Beispiel der

Donau o¨stlich von Wien. WSG Baden-Wu¨ rttem-

berg:53–68.

Dufour, S., and H. Pie´gay. 2008. Geomorphological

controls of Fraxinus excelsior growth and regener-

ation in floodplain forests. Ecology 89:205–215.

Eisenstat, D. M., and M. M. Caldwell. 1988. Seasonal

timing of root growth in favorable microsites.

Ecology 69:870–873.

Fahey, T. J., P. B. Woodbury, J. J. Battles, C. L. Goodale,

S. P. Hamburg, S. V. Ollinger, and C. W. Woodall.

2010. Forest carbon storage: ecology, management,

and policy. Frontiers in Ecology and the Environ-

ment 8:245–252.

Giese, L. A., W. M. Aust, R. K. Kolka, and C. C. Trettin.

2003. Biomass and carbon pools of disturbed

riparian forests. Forest Ecology and Management

180:493–508.

Giese, L. A., W. M. Aust, C. C. Trettin, and R. K. Kolka.

2000. Spatial and temporal patterns of carbon

storage and species richness in three South

Carolina coastal plain riparian forests. Ecological

Engineering 15:S157–S170.

Gloor, M., et al. 2009. Does the disturbance hypothesis

explain the biomass increase in basin-wide Ama-

zon forest plot data? Global Change Biology

15:2418–2430.

Gonza´lez, E. 2012. Seasonal patterns of litterfall in the

floodplain forest of a large Mediterranean river.

Limnetica 31:173–185.

Gonza´lez, E., M. Gonza´lez-Sanchis, A. Cabezas, F. A.

Comı´n, and E. Muller. 2010c. Recent changes in the

riparian forest of a large regulated Mediterranean

river: implications for management. Environmental

Management 45:669–681.

vwww.esajournals.org 13 October 2015 vVolume 6(10) vArticle 185

RIEGER ET AL.

Gonza´lez, E., M. Gonza´lez-Sanchis, F. A. Comı´n, and

E. Muller. 2012. Hydrologic thresholds for riparian

forest conservation in a regulated large Mediterra-

nean river. River Research and Applications 28:71–

80.

Gonza´lez, E., E. Muller, F. A. Comı´n, and M. Gonza´lez-

Sanchis. 2010b. Leaf nutrient concentration as an

indicator of Populus and Tamarix response to

flooding. Perspectives in Plant Ecology, Evolution

and Systematics 12:257–266.

Gonza´lez, E., E. Muller, B. Gallardo, F. A. Comı´n, and

M. Gonza´lez-Sanchis. 2010a. Factors controlling

litter production in a large Mediterranean river

floodplain forest. Canadian Journal of Forest

Research 40:1698–1709.

Gordon, W. S., and R. B. Jackson. 2000. Nutrient

concentrations in fine roots. Ecology 81:275–280.

Gurnell, A. 2014. Plants as river system engineers.

Earth Surface Processes and Landforms 39:4–25.

Horton, J. L., T. E. Kolb, and S. C. Hart. 2001.

Responses of riparian trees to interannual variation

in ground water depth in a semi-arid river basin.

Plant, Cell and Environment 24:293–304.

Houghton, R. A., J. I. House, J. Pongratz, G. R. van der

Werf, R. S. DeFries, M. C. Hansen, C. Le Que´re´, and

N. Ramankutty. 2012. Carbon emissions from land

use and land-cover change. Biogeosciences 9:5125–

5142.

IPCC. 2007. Summary for Policymakers in Climate

change 2007: the physical science basis. Contribu-

tion of Working Group I to the Fourth Assessment

Report of the Intergovernmental Panel on Climate

Change. Cambridge University Press, Cambridge,

UK.

Keith, H., B. G. Mackey, and D. B. Lindenmayer. 2009.

Re-evaluation of forest biomass carbon stocks and

lessons from the world’s most carbon-dense forests.

Proceedings of the National Academy of Sciences

USA 106:11635–11640.

Kiley, D. K., and R. L. Schneider. 2005. Riparian roots

through time, space and disturbance. Plant and Soil

269:259–272.

Kozlowski, T. 1971. Growth and development of trees.

Cambial growth, root growth, and reproductive

growth. Elsevier Science, Oxford, UK.

Lambers, H., and H. Poorter. 1992. Inherent variation

in growth rate between higher plants: a search for

physiological causes and ecological consequences.

Pages 187–261 in Advances in ecological research.

Volume 23. Elsevier, Amsterdam, The Netherlands.

Lehtonen, A., R. Ma¨kipa¨a¨, J. Heikkinen, R. Sieva¨nen,

and J. Liski. 2004. Biomass expansion factors (BEFs)

for Scots pine, Norway spruce and birch according

to stand age for boreal forests. Forest Ecology and

Management 188:211–224.

Leppa¨lammi-Kujansuu, J., M. Salemaa, D. B. Kleja, S.

Linder, and H.-S. Helmisaari. 2014. Fine root

turnover and litter production of Norway spruce

in a long-term temperature and nutrient manipu-

lation experiment. Plant and Soil 374:73–88.

Liu, C., C. J. Westman, B. Berg, W. Kutsch, G. Z. Wang,

R. Man, and H. Ilvesniemi. 2004. Variation in

litterfall-climate relationships between coniferous

and broadleaf forests in Eurasia. Global Ecology

and Biogeography 13:105–114.

Lu¨ ttge, U., M. Kluge, and G. Bauer. 1999. Botanik. 3.

Auflage. Wiley-VCH, Weinheim, Germany.

Magnussen, S., and D. Reed. 2004. Modeling for

estimation and monitoring. Chapter 5: carbon

content of vegetation. http://www.fao.org/forestry/

17111/en/

Manzanera, J. A., and M. F. Martı´nez-Chaco´n. 2007.

Ecophysiological competence of Populus alba L.,

Fraxinus angustifolia Vahl., and Crataegus monogyna

Jacq. used in plantations for the recovery of

riparian vegetation. Environmental Management

40:902–912.

McClaugherty, C. A., J. D. Aber, and J. M. Melillo.

1982. The role of fine roots in the organic matter

and nitrogen budgets of two forested ecosystems.

Ecology 63:1481–1490.

Megonigal, J. P., W. H. Conner, S. Kroeger, and R.

Sharitz. 1997. Aboveground production in south-

eastern floodplain forests: a test of the subsidy-

stress hypothesis. Ecology 78:370–384.

Megonigal, J. P., and F. P. Day. 1992. Effects of flooding

on root and shoot production of bald cypress in

large experimental enclosures. Ecology 73:1182–

1193.

Meier, C. E., J. A. Stanturf, and E. S. Gardiner. 2006.

Litterfall in the hardwood forest of a minor

alluvial-floodplain. Forest Ecology and Manage-

ment 234:60–77.

Mitsch, W. J., and J. G. Gosselink. 1993. Wetlands.

Wiley, Chichester, UK.

Naiman, R. J., and H. De´camps. 1997. The ecology of

interfaces: riparian zones. Annual Review of

Ecology and Systematics 28:621–658.

Pallardy, S. G., and T. T. Kozlowski. 2008. Physiology

of woody plants. Elsevier, Amsterdam, The Nether-

lands.

Pan, Y., et al. 2011. A large and persistent carbon sink

in the world’s forests. Science 333:988–993.

Persson, H. 1980a. Death and replacement of fine roots

in a mature scots pine stand. Ecological Bulletins

32:251–260.

Persson, H. 1980b. Spatial distribution of fine-root

growth, mortality and decomposition in a young

scots pine stand in Central Sweden. Oikos 34:77–

87.

Pie´gay, H., and S. A. Schumm. 2009. System approach-

es in fluvial geomorphology. Pages 105–134 in

G. M. Kondolf and H. Pie´gay, editors. Tools in

fluvial geomorphology. Wiley, Chichester, UK.

vwww.esajournals.org 14 October 2015 vVolume 6(10) vArticle 185

RIEGER ET AL.

Polgar, C. A., and R. B. Primack. 2011. Leaf-out

phenology of temperate woody plants: from trees

to ecosystems. New Phytologist 191:926–941.

Poorter, H., U

¨. Niinemets, L. Poorter, I. J. Wright, and

R. Villar. 2009. Causes and consequences of

variation in leaf mass per area (LMA): a meta-

analysis. New Phytologist 182:565–588.

Predick, K. I., S. E. Gergel, and M. G. Turner. 2009.

Effect of flood regime on tree growth in the

floodplain and surrounding uplands of the Wis-

consin River. River Research and Applications

25:283–296.

Pregitzer, K. S., and E. S. Euskirchen. 2004. Carbon

cycling and storage in world forests: biome

patterns related to forest age. Global Change

Biology 10:2052–2077.

Pregitzer, K. S., J. King, A. J. Burton, and S. Brown.

2000. Responses of tree fine roots to temperature.

New Phytologist 147:105–113.

R Development Core Team. 2011. R: a language and

environment for statistical computing. R Founda-

tion for Statistical Computing, Vienna, Austria.

Reich, P., and P. Bolstad. 2001. Productivity of

evergreen and deciduous temperate forests. Pages

245–283 in R. Saugier and H. Mooney, editors.

Terrestrial global productivity. Academic Press, San

Diego, California, USA.

Rieger, I., F. Lang, B. Kleinschmit, I. Kowarik, and A.

Cierjacks. 2013. Fine root and aboveground carbon

stocks in riparian forests: the roles of diking and

environmental gradients. Plant and Soil 370:497–

509.

Rieger, I., F. Lang, I. Kowarik, and A. Cierjacks. 2014.

The interplay of sedimentation and carbon accre-

tion in riparian forests. Geomorphology 214:157–

167.

Rood, S. B., J. H. Braatne, and F. M. R. Hughes. 2003.

Ecophysiology of riparian cottonwoods: stream

flow dependency, water relations and restoration.

Tree Physiology 23:1113–1124.

Rotkin-Ellman, M., K. Addy, A. J. Gold, and P. M.

Groffman. 2004. Tree species, root decomposition

and subsurface denitrification potential in riparian

wetlands. Plant and Soil 263:335–344.

Scheffer, F., P. Schachtschabel, and H.-P. Blume. 2010.

Lehrbuch der Bodenkunde. Springer Spektrum,

Heidelberg, Berlin, Germany.

Sieva¨nen, R., O. Salminen, A. Lehtonen, P. Ojanen, J.

Liski, K. Ruosteenoja, and M. Tuomi. 2014. Carbon

stock changes of forest land in Finland under

different levels of wood use and climate change.

Annals of Forest Science 71:255–265.

Simm, D. J., and D. E. Walling. 1998. Lateral variability

of overbank sedimentation on a Devon flood plain.

Hydrological Sciences Journal 43:715–732.

Tockner, K., F. Schiemer, and J. Ward. 1998. Conserva-

tion by restoration: the management concept for a

river-floodplain system on the Danube River in

Austria. Aquatic Conservation: Marine and Fresh-

water Ecosystems 8:71–86.

via donau–O

¨sterreichische Wasserstraßen-Gesellschaft

mbH. 2012. Die kennzeichnenden Wassersta¨nde

der o¨sterreichischen Donau. KWD 2010, Wien.

http://www.viadonau.org/fileadmin/content/

viadonau/02Infrastruktur/Dokumente/2015/KWD_

2010.pdf

Vogt, K. A., D. A. Publicover, J. Bloomfield, J. M. Perez,

D. J. Vogt, and W. L. Silver. 1993. Belowground

responses as indicators of environmental change.

Environmental and Experimental Botany 33:189–

205.

Vogt, K. A., D. J. Vogt, P. A. Palmiotto, P. Boon, J.

OHara, and H. Asbjornsen. 1996. Review of root

dynamics in forest ecosystems grouped by climate,

climatic forest type and species. Plant and Soil

187:159–219.

Williams, C. A., and D. J. Cooper. 2005. Mechanisms of

riparian cottonwood decline along regulated rivers.

Ecosystems 8:382–395.

Zak, D. R., W. E. Holmes, N. W. MacDonald, and K. S.

Pregitzer. 1999. Soil temperature, matric potential,

and the kinetics of microbial respiration and

nitrogen mineralization. Soil Science Society of

America Journal 63:575–584.

Zentralanstalt fu¨ r Meteorologie und Geodynamik.

2002. Klimadaten von O

¨sterreich 1971-2000.

http://www.zamg.ac.at/fix/klima/oe71-00/

klima2000/klimadaten_oesterreich_1971_frame1.

htm

Zentralanstalt fu¨ r Meteorologie und Geodynamik.

2013. Jahrbuch 2009, 2010 und 2011. Monats- und

Jahresu¨ bersichten der Messstationen, Wien. http://

www.zamg.ac.at/cms/de/klima/klimauebersichten/

jahrbuch

Zianis, D., P. Muukkonen, R. Ma¨kipa¨a¨, and M.

Mencuccini. 2005. Biomass and stem volume

equations for tree species in Europe. Silva Fennica

Monographs 4:1–63.

Zuur, A. F., E. N. Ieno, and C. S. Elphick. 2010. A

protocol for data exploration to avoid common

statistical problems. Methods in Ecology and

Evolution 1:3–14.

Zuur, A. F., E. N. Ieno, N. Walker, A. A. Saveliev, and

G. M. Smith. 2009. Mixed effects models and

extensions in ecology with R. Springer, New York,

USA.

vwww.esajournals.org 15 October 2015 vVolume 6(10) vArticle 185

RIEGER ET AL.

SUPPLEMENTAL MATERIAL

ECOLOGICAL ARCHIVES

Appendices A–K are available online: http://dx.doi.org/10.1890/ES14-00330.1.sm

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