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Biomass and productivity of fine and coarse roots in five tropical mountain
forests stands along an altitudinal transect in southern Ecuador
Gerald Mosera; Christoph Leuschnera; Marina Rödersteina; Sophie Graefea; Nathalie Soetheb; Dietrich
Plant Ecology, Albrecht-von-Haller Institute for Plant Sciences, University of Göttingen, Untere
Karspüle 2, 37073 Göttingen, Germany b Plant Nutrition and Fertilization, Humboldt University of
Berlin, Invalidenstraße 42, Berlin, Germany
Accepted uncorrected manuscript posted online: 27 August 2010
Online publication date: 27 August 2010
To cite this Article Moser, Gerald , Leuschner, Christoph , Röderstein, Marina , Graefe, Sophie , Soethe, Nathalie and

Hertel, Dietrich(2010) 'Biomass and productivity of fine and coarse roots in five tropical mountain forests stands along
an altitudinal transect in southern Ecuador', Plant Ecology & Diversity, 3: 2, 151 — 164, doi:
10.1080/17550874.2010.517788, First posted on: 27 August 2010 (iFirst)
To link to this Article: DOI: 10.1080/17550874.2010.517788

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Plant Ecology & Diversity
Vol. 3, No. 2, June 2010, 151–164

Biomass and productivity of fine and coarse roots in five tropical mountain forests stands
along an altitudinal transect in southern Ecuador

Gerald Mosera, Christoph Leuschnera*, Marina Rödersteina, Sophie Graefea, Nathalie Soetheb and Dietrich Hertela
Root production in tropical forests

aPlant Ecology, Albrecht-von-Haller Institute for Plant Sciences, University of Göttingen, Untere Karspüle 2, 37073 Göttingen,
Germany; bPlant Nutrition and Fertilization, Humboldt University of Berlin, Invalidenstraße 42, 10115 Berlin, Germany

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(Received 16 September 2009; final version received 19 August 2010)
Background: Data on below-ground production of tropical montane forests along elevation gradients are scarce.
Aims: To determine fine, coarse and large root biomass and productivity along a 2000 m elevation transect.
Methods: In five south Ecuadorian mountain forests along a transect from 1000 to 3000 m above sea level, fine (< 2 mm
diameter), coarse (2–50 mm) and large root biomass (> 50 mm) were analysed by soil coring and excavation of soil pits.
Fine root production was estimated synchronously by three different approaches (sequential soil coring, the ingrowth core
method, and the mini-rhizotron technique). Coarse and large root production was estimated by recording diameter increment
using dendrometer tapes.
Results: Fine root biomass increased four-fold between 1000 and 3000 m; coarse and large root biomass doubled. The three
approaches for estimating fine root production yielded highly divergent results, with the mini-rhizotron approach giving the
most reliable data, and indicating a significant increase in fine root production with elevation.
Conclusions: Our results indicate a marked carbon allocation shift from above- to below-ground towards higher elevations,
which is probably a consequence of increasing nutrient limitation of tree growth with increasing elevation.
Keywords: root biomass; root decomposition; root necromass; root production; soil chemistry; temperature; tropical rainforest

Few studies in the past have addressed the contribution
of root systems to the productivity of tropical forest ecosystems, and when they have done, methodological comparisons have dominated the discussion. A variety of
different approaches to determine fine root production
have been used, the most common being the ‘ingrowth
core’ and the ‘sequential soil coring’ methods, recently
supplemented by the mini-rhizotron technique. Reflections on the growth rate of coarse and large roots in tropical forests have been entirely hypothetical (Clark et al.
2001a). As a result the below-ground production has
played a minor role in most publications on net primary
production in tropical forests, or only rough estimates
have been given.
The change in productivity of tropical moist forests
along altitudinal transects has been studied in a number of
regions, including Malaysia (Kitayama and Aiba 2002),
Puerto Rico (Weaver and Murphy 1990; Wang et al. 2003)
and Hawai’i (Raich et al. 1997). However, in all of these
studies only above-ground net primary production (ANPP)
has been assessed. Since empirical data based on measurements in tropical montane forests are few, below-ground
productivity has so far been included only as a constant
portion of ANPP (Wang et al. 2003).
A review by Clark et al. (2001b) gave a range for
below-ground net primary production (BNPP) in tropical forests of 1.7 to 21.7 Mg C ha–1 year–1 (20 to 120% of ANPP),
*Corresponding author. Email:
ISSN 1755-0874 print/ISSN 1755-1668 online
© 2010 Botanical Society of Scotland and Taylor & Francis
DOI: 10.1080/17550874.2010.517788

which demonstrates the importance of BNPP in productivity estimates. Such a wide range is a reflection of the fact
that our knowledge on root production in tropical forest
ecosystems is very limited, and an adequate model is not
yet available to predict the ratio of above- to below-ground
production along environmental gradients such as precipitation, temperature and nutrient availability. Until
recently, the lack of precise data on root production in
tropical montane forests has generated considerable uncertainties about carbon (C) balance and turnover in these
We have conducted a comprehensive study on tree
root mass and root dynamics in five tropical mountain
forest stands in southern Ecuador, firstly to quantify the
biomass of fine and coarse roots along an altitudinal
transect from 1000 to 3000 m elevation above sea level
(a.s.l), secondly to compare estimates of fine and coarse
root production by using three independent methods, and
finally to investigate the influence of elevation-associated
changes in environmental factors on root biomass and root
Material and methods
Study sites
The study was conducted on the eastern slopes of the south
Ecuadorian Andes, about 500 km south of the Equator.
Five forest stands, at 1050, 1540, 1890, 2380 and 3060 m


G. Moser et al.

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a.s.l., were selected in the Podocarpus National Park, Loja
Province, and the adjacent Reserva Biológica San Francisco, Zamora-Chinchipe Province. Four stands were situated on moderately steep slopes (26° to 31°) facing northeast to north-west, while one stand was located close to a
ridge (10° slope angle). Structurally homogeneous forest
stands without canopy gaps were selected, representative
of the forest type at a given elevation in terms of tree species composition and forest structure. Comprehensive floristic data had been collected in the region by Homeier et
al. (2008). However, the tree species inventories remained
incomplete, in particular in the stands at 1050 and 1540 m
in which some tree individuals were identified only to
genus or family level.
The relative abundance of plant families in the communities points to a more or less continuous species turnover from the lower to the upper montane forests (Table 1).
The Melastomataceae was the only family to occur at all
five elevations. Five other families were present in four of
the five stands (Myrtaceae, Lauraceae, Araliaceae, Rubiaceae
and Chloranthaceae). In contrast, all other recorded families
showed clear altitudinal preferences by occurring only at

one or two (or, in a few cases, three) elevations. The genus
Miconia (Melastomataceae) was exceptional by appearing
in all five stands and M. punctata occurred as a prominent
species in three (1, 2 and 3). Another species with a rather
broad elevational range was the Melastomataceae Graffenrieda emarginata, which dominated Stand 3 and also
appeared in Stand 4.
All stands showed no, or only minimal, evidence of
human influence. The uppermost stand was located close
to the treeline, which in this region is situated at an unusually low elevation (3200–3400 m a.s.l.). A forest line
depression is characteristic of the Amotape–Huancabamba
Floristic Zone between 3° S and 7° S, where the lack of
high Andean peaks in the drier western Cordillera leads to
the absence of a high altitude Polylepis belt (Richter et al.
A detailed environmental characterisation of the five
stands is given in Table 2. Mean air temperature (measured
at 1.5 m height within the forest stands), and mean soil
temperature in the organic layer and in the mineral topsoil
(10 cm), were very similar and decreased by 0.5 °C per
100 m elevation. The absolute temperature minimum in

Table 1. Percentage contribution of plant families to the total number of stems in the five study plots along an altitudinal transect from
1050 m (Stand 1) to 3060 m (Stand 5) elevation in southern Ecuador.
Plant families
Not determined

Stand 1

Stand 2

Stand 3














Stand 4

Stand 5

Important genera
Axinea, Graffenrieda, Miconia
Ocotea, Aniba
Cinchona, Palicourea
Purdiaea nutans




A total of 80 trees were surveyed per plot; species determination were carried out by J. Homeier, University of Göttingen.

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Root production in tropical forests
the organic layer at 3060 m was 8.1 °C, and minimum air
temperature was 3.1 °C. Annual rainfall was similar in the
three lowermost stands (around 2000 mm), while the two
uppermost stands received remarkably high amounts of
rain (4500–5000 mm). The mean water content of the
organic layer and the mineral topsoil increased linearly
with elevation. The absolute minima of soil water content
were < 5% in the organic layer of Stands 1–3, while the
organic layer of the two uppermost stands remained wet
throughout the whole period of measurement (May 2003–
April 2004). The mineral topsoil remained relatively moist
over the year, not only in Stands 4 and 5 but also in the
lowermost stands (Table 2).
The soils of the two lowermost stands were classified
as Alumic Acrisols derived from granodiorites. The
Gleyic Cambisols of Stands 3 and 4 and the Podzols of
Stand 5 were derived from shale, quartzite and sandstone. The depth of the organic layer increased almost
tenfold between 1050 m and 3060 m and was accompanied by a three-fold increase in the C:N ratio in the
organic layer and the mineral topsoil. The pH of the mineral soil was low, and decreased with elevation. The base
saturation of the mineral topsoil was highest in Stand 5,
close to the forest line (23%), and was two to three times


lower in Stands 1 to 4 (data on soil type and chemistry
provided by Iost 2007).
Above-ground forest structure changed noticeably
with elevation. Mean canopy height decreased three-fold
and mean diameter at breast height (DBH) about 2.5-fold
between 1000 m and 3000 m (Table 3), whereas stem density increased from 968 to 8317 ha–1 (Moser et al. 2008).
Basal area showed no significant altitudinal trend, but
reached a maximum at 3060 m, where stem density was
very high. Leaf area index (LAI) decreased nearly threefold along the slope. Further details of the above-ground
structure of the five forest stands are given by Moser et al.
(2007, 2008).
Biomass and production of coarse and large roots
In order to measure the biomass of coarse and large roots,
12 to 16 soil pits (40 cm × 40 cm) were dug in randomised
locations by cutting the dense root systems with a hand
saw and then excavating the mineral soil from the surface
to a depth of 50 cm. Only in cases where the distance to
the next large tree (DBH > 30 cm) was < 1 m, did we deviate from this pattern. All root biomass (live roots) and necromass (dead roots) with a root diameter > 2 mm was

Table 2. Location data and physiographic characteristics (mean, range) for the five stands in southern Ecuador.

Elevation (m)
Slope (°)
Temperature (°C):
Organic layer
Mineral soil (10 cm)
Rainfall (mm year–1)
Soil type
Soil water content (vol%):
Organic layer
Mineral soil
Organic layer depth (mm)
pH (CaCl2) (Ah)
C:N (L/Of1)
Base saturation (Ah) (%)

Stand 1

Stand 2

Stand 3

Stand 4

Stand 5

S 04° 06′ 54″
W 78° 58′ 02″

S 04° 06′ 42″
W 78° 58′ 20″

S 03° 58′ 345″
W 79° 04′ 648″

S 03° 59′ 19″
W 79° 04′ 55″

S 04° 06′ 71″
W 79° 10′ 581″

19.4 (11.5 – 30.2)
20.0 (14.4 – 28.7)
19.4 (14.4 – 27.4)
c. 2230

17.5 (11.2 – 26.7)
18.9 (16.1 – 20.6)
18.5 (17.3 – 19.2)
c. 2300

15.7 (7.9 – 29.4)
16.0 (11.7 – 18.8)
16.4 (15.3 – 18.2)
c. 1950

13.2 (7.0 – 25.1)
14.9 (13.3 – 16.6)
13.0 (11.6 – 13.9)
c. 5000

9.4 (3.1 – 18.8)
9.7 (8.1 – 10.8)
9.8 (8.7 – 10.7)
c. 4500

9.9 (4.4–16.0)
29.7 (15.3–38.5)

12.9 (3.4–23.9)
30.3 (20.4–43.5)

11.6 (3.6–22.3)
35.4 (27.4–44.7)

34.0 (23.8–39.8)
44.7 (35.7–48.7)

45.3 (30.5–61.7)
49.1 (39.5–59.5)

Air temperature (at 1.5 m height inside the stands) and soil temperature (annual mean and range in parentheses) were measured between May 2003 and
April 2004. Rainfall was recorded in gaps at 1050, 1950, 2680 and 3170 m and extrapolated to the study stands (data from P. Emck, University of Erlangen: Stands 3–5, and our own measurements). Volumetric soil water content was measured continuously using TDR probes in the organic layer and the
mineral soil at a depth of 10 cm (annual means and extremes). pH (CaCl2) of the mineral topsoil (0–30 cm), C:N ratio of organic layer (L/Of1), base saturation (Ah) and soil type were determined by Iost (2007).

Table 3. Above-ground forest structure of the five stands studied. Values are means, ± SE where applicable.

Canopy height (m)
LAI (m2 m–2)
DBH (cm)
Basal area (m2 ha–1)

Stand 1

Stand 2

Stand 3

Stand 4

Stand 5

6.0 ± 0.4a
17.3 ± 1.3a

5.4 ± 0.4a
11.5 ± 0.6b

5.7 ± 0.5a
12.2 ± 0.8b

2.8 ± 0.2b
9.8 ± 0.6c

2.2 ± 0.2c
7.2 ± 0.4d

Canopy height, DBH and basal area are from Moser et al. (2008); LAI from Moser et al. (2007). Different letters indicate statistically significant differences
between the stands (P < 0.05).


G. Moser et al.

extracted, and the root material was separated into an
organic layer and five mineral soil horizons (0–10, 10–20,
20–30, 30–40 and 40–50 cm). In the laboratory of the
Estación Científica San Francisco (ECSF), the roots were
washed and sorted into five different diameter classes
(0.2–1, 1–2, 2–5, 5–10 and > 10 cm) and dried to constant
mass at 70 °C.
The radial wood increment of coarse and large roots
was measured to an accuracy of 0.01 cm (dendrometer
type D1, UMS GmbH Munich, Germany) using tapes of
Astralon. In each stand, 20 root segments close to the soil
surface were equipped with tapes. The increase in diameter was recorded every three months between April 2003
and September 2004. The original diameter of the roots
varied between 3 and 32 cm. The volume increment of the
20 roots investigated per plot was extrapolated to the level
of the stand, based on information about coarse and large
root biomass, root diameter distribution and stem density
in the five stands, enabling estimation of coarse and large
root production overall.

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Fine root biomass and production
Fine root biomass (live and dead) was measured by soil coring at 15 randomly selected locations per stand to a soil
depth of 50 cm. To quantify fine root production, three different approaches were adopted:

• sequential soil coring (Vogt and Persson 1991) in

combination with a maximum–minimum calculation
procedure (Edwards and Harris 1977; McClaugherty
et al. 1982), and sequential coring in combination
with a compartmental flow calculation (McClaugherty
et al. 1982; Santantonio and Grace 1987);
• the ingrowth core method (Persson 1980; Powell
and Day 1991; Majdi 1996); and
• the mini-rhizotron technique (Hendrick and Pregitzer
1992; Hendrick and Pregitzer 1996; Nadelhoffer
Sequential soil coring
Sequential coring was conducted in 20 randomly selected
subplots (2 m × 2 m) for each stand. In each subplot, one
soil sample was taken on a given sampling date using a
steel corer (3.5 cm diameter) in the organic layer and in the
uppermost 30 cm of the mineral soil. Sampling took place
between October 2001 and August 2002 (Stands 3–5) and
between April 2003 and February 2004 (Stands 1–2), at
intervals of 42 days, making eight samples in total.
A preliminary investigation to a depth of 60 to 80 cm
showed that the organic layer and the mineral soil at a depth
of 30 cm contained about 75% or more of the total profile of
tree fine root biomass. We therefore decided to include within
our investigation the mineral soil from 0 to 30 cm in depth
plus the organic layer, henceforth referred to as ‘profile total’.
The extracted soil cores were separated into organic and
mineral strata, transferred to plastic bags and transported to

the laboratory at the ECSF, where the samples were stored
at 4° C and processed within 30 days.
The processing and separation into living fine root
(diameter < 2 mm) biomass and dead fine root necromass
was carried out according to the method described by van
Praag et al. (1988) and modified by Hertel and Leuschner
(2002). The samples were soaked in water and soil residues removed using a sieve (0.25 mm mesh). Fine root
segments longer than 10 mm were removed by hand. Live
and dead rootlets were distinguished under a stereomicroscope by colour, root elasticity and the degree of cohesion
of cortex, periderm and stele. A dark cortex and stele, a
white but non-turgid cortex and stele, or the existence only
of the periderm, were used as indicators for root death
(Persson 1978; Leuschner et al. 2001).
Six out of 20 soil samples per plot and horizon were
subjected to a detailed analysis of fine root particles < 10
mm length; this fraction was considered likely to account
for a large proportion of the total fine root necromass
(Bauhus and Bartsch 1996; Hertel 1999). After manually
extracting the long fine roots, the residue of the sample
was evenly spread on a piece of filter paper (730 cm2)
divided into 36 squares of 4 cm × 4 cm in size. Six of the
squares were randomly selected and the quantity of fine
root fragments was assessed under a microscope. The dry
mass of small dead rootlets was extrapolated to the entire
sample by taking the ratio of the small dead rootlets to the
large dead fine roots (> 10 mm length), established from a
sub-sample. Fine root biomass and necromass samples
were dried at 70 °C (48 h) and the dry mass was used to
calculate the total of living and dead fine root mass in the
stand, either at a given sampling date or as an annual average.
Annual fine root production was calculated from the
sequential coring data by the maximum–minimum
method (Edwards and Harris 1977; McClaugherty et al.
1982), taking the difference between the maximum and
minimum of the sum of the fine root biomass plus necromass. The calculation was repeated separately for each of
the 20 subplots per stand to assess asynchronous fine root
growth within a given stand. The difference between sampling dates, showing the lowest and highest total fine root
mass, measured for every subplot of a stand, allowed production to be estimated. This approach neglects synchronous events of fine root production and death that might
have occurred between the dates with the highest and
lowest root mass, and could therefore lead to an underestimation of fine root turnover (McClaugherty et al.
1982; Aber et al. 1985; Gower et al. 1992; Publicover and
Vogt 1993).
Since the maximum–minimum calculation method might
not be appropriate for tropical forest ecosystems with low
or nonexistent seasonality of fine root growth, we also
applied the alternative compartmental flow method of
calculation (McClaugherty et al. 1982; Santantonio and
Grace 1987). This approach allows the calculation of fine
root production during periods of synchronous growth and
mortality, and also considers losses of necromass due to
decomposition, by applying the decision matrix of Fairley

Root production in tropical forests
and Alexander (1985). Fine root production was quantified
from the changes in live and dead root mass over 42-day
intervals, and by subsequently adding the losses due to
fine root litter decay (see below) over these periods.

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Ingrowth cores
In April 2003 an ingrowth core study was established. In
each of the five stands, 20 soil cores (55 mm diameter and
25 cm depth) were taken from the randomly distributed
subplots used for the sequential coring approach. All visible fine roots in the soil were carefully removed by hand
and the soil material was reinserted into the holes and
compressed to about the original soil density. Holes were
filled by adding soil from additional cores, thus replacing
the volume of the roots extracted. Organic layer and mineral topsoil samples were treated separately. The cleaned
material was filled back into the holes to re-establish reasonably natural soil conditions. The ingrowth cores were
marked with PVC tubes and recovered after 15 months
using the same soil corer as used originally. The soil was
separated into organic and mineral fractions and placed in
polyethylene bags. To estimate the impact on fine root
growth caused by root injury during core removal, 10
additional ingrowth cores were taken per plot. Two of
these were re-sampled in each plot after 6, 12, 18, 24 or 30
weeks and the fine root biomass ingrowth determined.
In the ECSF laboratory the soil samples were washed
and all the fine rootlets (> 10 mm length) were extracted
by hand, washed and dried (70 °C, 48 h). The study with
sequential re-sampling of ingrowth cores indicated that
fine root ingrowth into the cores began about three months
after the start of the experiment. It was thus assumed that
the fine root biomass detected in the cores after 15 months
represented a fine root growth period of 12 months. As the
depth of the ingrowth cores was 25 cm, production estimates obtained using this method applied only to the
organic layer in the high-elevation stands, which had thick
humus layers. Nevertheless, with the fine root biomass
data from the organic layer and the mineral topsoil, the
ingrowth core production estimates could be extrapolated
to the soil profile covered by the sequential coring
approach (organic layer plus mineral soil to 30 cm).
As a further independent method for studying fine root
dynamics, 10 transparent mini-rhizotron tubes with an
external diameter of 70 mm were installed in each stand in
June 2005. These were placed perpendicular to the soil
surface and wherever possible inserted at a depth of about
40 cm. Only the first 10 cm below the soil surface was
considered for the assessment of fine root dynamics, as in
a number of cases the very high stone content of the mineral soil at the lowermost stand did not allow the tubes to
be installed more deeply. To monitor root growth, a root
scanning system (CI–600 Root Growth Monitoring System,
CID Inc., USA) was employed at monthly intervals until


January 2007. In order to avoid artefacts caused by disturbance during installation of the tubes, only the data from
November 2005 onwards were considered for analysis.
The images were analysed using the programme WinRHIZO
Tron (Régent, Quebec, Canada). Only fine roots were used
for the analysis. Relative root length production and relative root loss were calculated by relating root length production or root loss between two observation dates to the
root length visible at the previous measuring date. Extrapolation of these data to a full year allowed estimation of
average annual root production and loss rates, root turnover rate as a percentage of the standing stock, and root longevity (days) of the visible fine root population in the
rhizotron tubes (Nadelhoffer 2000). From turnover rates in
the uppermost 10 cm and biomass data from the organic
layer and mineral topsoil (0–30 cm), annual fine root production was calculated for the five stands.
Fine root litter decomposition
Decomposition of fine root litter was studied using two
different litter bag studies, largely following the protocol
proposed by Fahey et al. (1988). In the first of the studies
we investigated the decomposition rate of dead fine root
material at the site of origin. During March 2003 live fine
root material was sampled from the organic layer of each
stand, cleaned of soil residues and 5 g fresh weight of this
material inserted into litter bags (nylon, 10 cm × 10 cm,
mesh 1 mm, n = 12). Additional fine root material was
immediately dried for determination of water content. The
litter bags were exposed within the organic layer at random locations within each plot and covered by a thin layer
of leaf litter. After 12 months’ exposure in the field, the
litter bags were recovered, and the remaining undecomposed roots carefully cleaned of soil residues, dried and
weighed. In a second litter bag study, starting January 2004,
we sampled live fine roots from the mid-elevation Stand 3
(1890 m a.s.l.) and exposed this material in the five stands
for six months to estimate the decomposition rate in a
standardised manner, independent of differences in root
properties among the five stands. In each study the decomposition rate was calculated from the difference between
the initial and the remaining root mass in the litter bag.
To obtain information on root chemistry, which determines the ability of fine roots to decompose, the C:N ratio
of fresh fine root biomass to necromass (n = 40) was
measured using a CN–Analyser (Vario EL III, Fa. Elementar, Hanau, Germany) and the polyphenol concentration
in fine roots (n = 10) from the organic layer was determined by photometry (DU 640 Spektralphotometer, Fa.
Beckmann, Germany, data provided by M. Unger). Cleaned
fresh fine root material for the analysis was frozen at
–20 °C. After the samples had been transported to Göttingen under continuous cooling they were ground to powder
under liquid nitrogen in a mortar. For the assessment of
soluble and insoluble tannin concentration, a repeat
procedure was conducted by suspending the sample in
methanol (twice) and subsequently in acid–butanol and


G. Moser et al.
calculations were carried out using Xact software (SciLab,
Hamburg, Germany, version 8.0).

FeNH4(SO4)2.12H2O, followed by incubation at a range
of temperatures (initially in an ultra-sound bath) and centrifuged (4500 rpm). Proanthocyanidin was used as standard and measured alternately with the sample solutions at
550 nm wavelength. A similar procedure was employed to
determine the concentration of soluble and insoluble phenols. Folin–Ciocalteu’s phenol and Na2CO3 solution were
used as reagents for soluble phenols; the standard solution
was catechin (Fluka, Buchs, Switzerland). Insoluble phenols were detected after the addition of n-hexane (Merck,
Darmstadt, Germany) and NaOH; the standard solution
contained p-coumaric acid (Fluka, Buchs, Switzerland). To
determine the concentration of soluble and insoluble phenols, the sample solutions were examined in a photometer
at 765 nm wavelength, alternating with the respective
standard solutions. All the concentration data obtained
were recorded relative to the fresh weight of a sample.

Root biomass distribution
Total below-ground biomass (fine, coarse and large roots)
was largest at the highest elevation stand, both coarse and
large root biomass being significantly higher than those in
the lower stands. Between 1050 and 2380 m a.s.l., total
estimated root biomass ranged from 26.1 to 39.4 Mg ha–1
(Table 4).
The increase in total root biomass with elevation was
mainly due to a conspicuous increase in root mass within
the organic layer, which itself increased about nine-fold in
thickness. Most of the root biomass in Stands 2–5 was
concentrated in the organic layer, reaching 83% of the
total profile in Stand 4 and 77% in Stand 5. Below a depth
of 30 cm in the mineral soil only a very few coarse and
large roots were found. Total root biomass correlated with
all seven environmental factors tested, but the closest
relationship existed between root mass and soil C:N ratio
and root mass and soil proton concentration (Table 5).
The contribution of fine root to total root biomass
increased with elevation. Similarly to total root mass, fine
root biomass also correlated significantly with all the
environmental parameters tested, apart from precipitation.
Fine root biomass increased linearly with elevation, while
necromass increased exponentially (Figure 1). In the two
lowermost stands, fine root biomass and necromass were
similar; in contrast, at the highest altitude necromass
exceeded biomass by a factor of 2.7. Coarse and large root
biomass showed a high spatial variability among the
stands, particularly in the lowermost stands, which may

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Statistical analysis
Differences in root biomass, root production and decomposition rates among the five stands were analysed by the
Kruskal–Wallis test and the Mann–Whitney two-sample
test (U-test) using the package SAS (SAS Institute, Cary,
NC, USA, version 8.2).
Linear and simple non-linear regression analysis was
used to identify the significance of elevation, mean air
temperature, annual precipitation, soil moisture and proton
concentration in the mineral soil, or the C:N ratio of the
organic layer, on root biomass and root production
estimates. Additional regression analysis was performed
on the relationship between the polyphenol content or
C:N ratio of fine roots and litter decomposition rate. The

Table 4. Means ± SE of standing biomass of coarse and large roots (diameter > 2 mm) and living fine roots (< 2 mm) from soil coring
in the organic layer (variable in depth), mineral soil (30 cm) and the total profile to 30 cm depth in Mg ha–1 in the five forest stands.
Coarse and large roots n = 12; fine roots n = 15.
Stand 1
Coarse + large roots

Total root mass

Stand 3


Stand 4


22.2 ±
8.1 ±
30.7 ±
3.6 ±
2.2 ±
5.6 ±

2.2 ±
26.8 ±
29.4 ±
0.5 ±
2.2 ±
2.7 ±

profile total
profile total
profile total

Fine roots

Stand 2


Stand 5


12.3 ±
4.7 ±
19.6 ±
2.4 ±
3.3 ±
6.2 ±

37.8 ± 4.3b
8.5 ± 2.3a
51.9 ± 4.7c
6.5 ± 0.3d
4.8 ± 0.3c
10.8 ± 0.6c

24.0 ±
3.0 ±
32.7 ±
3.6 ±
2.8 ±
6.3 ±

Different letters indicate statistically significant differences (P < 0.05).

Table 5. Results of correlation analyses between three root biomass fractions and stand climatic and edaphic variables.









Soil moisture




Soil acidity



C:N ratio



Coarse + large roots 0.35 0.13 0.149 0.39 0.18 0.131 0.35 0.14 0.145 0.34 0.12 0.153 0.61 0.48 0.059 0.59 0.46 0.064
Fine roots
0.90 0.87 0.006 0.89 0.86 0.007 0.37 0.16 0.140 0.71 0.61 0.036 0.85 0.80 0.012 0.83 0.77 0.015
Total root mass
0.69 0.58 0.040 0.73 0.64 0.032 0.68 0.57 0.043 0.91 0.82 0.043# 0.84 0.78 0.014 0.90 0.87 0.006
Statistically significant results are printed in bold (P < 0.05); #, non–linear relationships.

Root production in tropical forests




Mass loss per year (%)

Elevation (m a.s.I.)





Standard material


Local material





adj = 0.87, P = 0.006


adj = 0.99, P = 0.002



Fine root biomass (g m–2) Fine root necromass (g m–2)


Figure 2. Annual mean ± SE fine root decomposition rate
expressed as percentage mass loss on initial fresh root mass in
litter bags along the elevation transect. Local root material was
exposed for 12 months (r2 = 0.83, P = 0.015); standard root material
from Stand 3 at 1850 m was exposed for 6 months (r2 = 0.56,
P = 0.073); n = 12 for both.

Figure 1. Mean ± SE fine root biomass and necromass versus
elevation along the transect and results of the regression analysis. Values are profile totals (0–50 cm of mineral soil and
organic layer, n = 15 samples each).

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Elevation (m a.s.l)

partly bias the overall stand-level estimates of root biomass in the study. The largest quantities of coarse and
large root biomass were present in Stand 5 (52 Mg ha–1),
and the lowest in Stand 3 (20 Mg ha–1, Table 4). The biomass of large diameter roots showed no significant relationship with any of the environmental variables examined
(Table 5).
Fine root decomposition
The decomposition rate of fresh fine root material when
exposed at the site of origin was very similar at the three
lowermost elevations, but decreased in the two uppermost
stands to about a third of the rate of that at 1050 m (Figure 2).
The potential decomposition rate, determined by exposing
standard material from Stand 3, was higher in all stands
(except Stand 3) than the decomposition rate of the local
root material. The decomposition of standard root material
showed a trend towards a decrease (P = 0.07) with
The concentration of soluble phenols in fine roots
increased significantly with elevation (Table 6), as did the
concentration of insoluble phenols. The concentration of

soluble tannin in fine roots remained invariant from 1050
to 2350 m, and reached a maximum at 3060 m, while
insoluble tannin concentration showed no significant trend
along the transect. A correlation analysis showed that the
decomposition rate of local root material decreased significantly, with higher soluble phenol (r2 = 0.96, P = 0.002)
and soluble tannin concentration (r2 = 0.71, P = 0.037),
and also with an increasing C:N ratio in the root material
from the organic layer of each stand (biomass: r2 = 0.90,
P = 0.006; necromass: r2 = 0.94, P = 0.003).

Root production
The annual production of coarse and large roots (> 2 mm)
was estimated at about 0.2 Mg ha–1 year–1 in Stands 1, 3
and 4, and was significantly higher in Stands 2 and 5
(Table 7). None of the five environmental variables investigated, nor elevation, showed correlation with coarse and
large root production.
Fine root production, estimated by sequential coring
combined with the maximum–minimum calculation procedure, increased more than ten-fold along the transect

Table 6. Mean + SE polyphenol concentration of fine root biomass and C:N ratio of fine root bio- and necromass of the organic layer
in the soil of five forest stands.

Polyphenols (mg
fresh biomass)
C:N ratio
Fine root biomass
Fine root necromass

Stand 1

Stand 2

Stand 3

Stand 4

Stand 5

1.7 ± 0.4a
4.2 ± 0.8a
4.8 ± 1.9a
50.4 ± 8.2ab

2.3 ± 0.3a
12.9 ± 2.3b
6.9 ± 1.1a
57.3 ± 5.6b

2.3 ± 0.5a
7.4 ± 1.6ab
4.9 ± 1.3a
51.0 ± 7.2ab

3.9 ± 1.2b
7.6 ± 1.8ab
6.0 ± 1.0a
34.4 ± 4.2a

4.9 ± 0.7b
19.8 ± 2.6c
14.5 ± 1.7b
45.8 ± 7.2ab

28.2 ± 1.0a
23.6 ± 1.9a

34.2 ± 0.6b
26.9 ± 0.5a

43.4 ± 0.9c
33.1 ± 0.8b

55.2 ± 1.2d
44.2 ± 1.0c

91.1 ± 3.3e
60.1 ± 1.5d

Polyphenols: n = 10; C:N, n = 40; different letters indicate statistically significant differences between the forest stands (P < 0.05).


G. Moser et al.

Table 7. Mean + SE of stand level estimates of coarse and large (> 2 mm) root growth in the organic layer and the mineral soil
(0–50 cm) of five stands, extrapolated from increment rates of 20 roots per stand and coarse and large root biomass data (in Mg ha–1).

profile total

Stand 1

Stand 2

Stand 3

Stand 4

Stand 5

0.01 ± 0.003a
0.16 ± 0.04α
0.17 ± 0.04A

0.58 ± 0.08b
0.21 ± 0.06α
0.79 ± 0.14B

0.16 ± 0.02c
0.06 ± 0.02β
0.22 ± 0.03A

0.20 ± 0.04c
0.03 ± 0.01β
0.23 ± 0.04A

0.72 ± 0.05b
0.16 ± 0.03α
0.89 ± 0.08B

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Different letters indicate statistically significant differences between the forest stands (P < 0.05).

(Table 8) and showed the strongest positive correlation
with the C:N ratio in the organic layer and the proton concentration in the mineral soil (Table 9). The maximum–
minimum production values also increased significantly
with mean soil water content, but decreased with temperature. The production estimates correlated negatively with
LAI (r2 = 0.85, P = 0.012) and annual leaf production (r2 =
0.087, P = 0.010; data from Moser et al. 2007). Sequential
coring, combined with compartmental flow calculation,
yielded unrealistically high values in Stands 3, 4 and 5,
and these data were disregarded. In contrast to sequential
coring, the ingrowth core approach resulted in relatively
low production estimates, except for Stands 1 and 2, and
indicated an absolute minimum of fine root production at
1050 m elevation, a maximum at 1540 m and then a
decrease towards 3060 m (Table 8). The production data
using this approach did not correlate well with any of the
environmental variables tested (Table 9).
A statistically supported relationship between ingrowth
core-derived root production and leaf production appeared
when Stands 2–5 alone were included in the analysis
(LAI: r2 = 0.71, P = 0.080; annual leaf production: r2 = 0.81,
P = 0.050).
The mini-rhizotron data, combined with the root
biomass totals of the 0–30 cm profile, showed a greater
than four-fold increase in fine root production with
Total BNPP was defined as the sum of fine, coarse and
large root production, the first component being calculated
alternately using the approaches mentioned above (Figure 3).

BNPP obtained from the maximum–minimum calculation
or from mini-rhizotron data increased ten- and fourfold,
respectively, with elevation. Total root production estimated from ingrowth cores was somewhat higher in the
two lowermost stands than from the results obtained by the
other approaches. Whereas the BNPP estimates based on
the maximum–minimum or the compartmental flow calculation, or on the mini-rhizotron data, correlated with soil C:N
ratio, soil acidity, soil moisture and temperature (or elevation), the ingrowth core-based data were not significantly
dependent on any of these variables, nor was rainfall
related to any BNPP estimate (Table 9).
Effect of change in altitude on root biomass, and its causes
Evidence of increasing fine root biomass with elevation in
tropical mountain forests has previously been reported
from Mount Kinabalu, Malaysia (Kitayama and Aiba
2002), and it supports our result of a greater than threefold
increase in fine root biomass and a doubling of total root
mass between 1050 m and 3060 m elevation. Moreover,
a comprehensive review of fine root biomass data from
tropical moist forests compiled by Hertel and Leuschner
(2010), which includes data from the present study, suggests an exponential increase with elevation. However, the
fine root biomass recorded at Mount Kinabalu was at most
elevations greater than in the Ecuadorian transect at similar altitudes. Particularly high fine root biomass has been
found in a tropical montane oak forest in Costa Rica at

Table 8. Means + SE of biomass production of fine roots (Mg ha–1 year–1) in the organic layer and the mineral soil (0–30 cm) as
estimated with three different methods (and two different calculation procedures in the sequential coring approach).
Sequential coring
(Comp. flow)
Sequential coring
Ingrowth cores

Soil horizon
profile total
profile total
profile total
profile total

Stand 1
0.99 ±
1.17 ±
2.15 ±
1.44 ±
0.50 ±
1.94 ±
0.76 ±
2.86 ±
3.62 ±
0.41 ±
1.87 ±
2.28 ±


Stand 2
2.72 ±
1.00 ±
3.72 ±
4.79 ±
1.30 ±
6.09 ±
6.08 ±
2.98 ±
9.06 ±
1.95 ±
1.22 ±
3.16 ±


Stand 3
14.49 ±
7.70 ±
22.19 ±
4.52 ±
2.24 ±
6.76 ±
3.38 ±
3.64 ±
7.02 ±
1.16 ±
1.58 ±
2.97 ±

Different letters indicate statistically significant differences between the forest stands (P < 0.05).


Stand 4
21.14 ±
14.64 ±
35.78 ±
7.89 ±
4.61 ±
12.05 ±
3.55 ±
2.55 ±
6.10 ±
2.12 ±
1.63 ±
3.72 ±


Stand 5
32.98 ± 0.93e
42.62 ± 1.68d
75.60 ± 2.14e
10.87 ± 1.42d
11.06 ± 1.27e
21.93 ± 2.15d
2.26 ± 0.29c
1.52 ± 0.20a
3.78 ± 0.49a
5.71 ± 0.76d
4.26 ± 0.57b
9.40 ± 1.32c

Ing Cor
Ing Cor

Coarse + large roots
Fine rootsMax–Min



BNPP (Mg ha–1 yr–1)

Coarse and large root production was determined by diameter increment measurement at 20 root segments per plot. Fine root production was estimated by sequential coring combined with a maximum–minimum
calculation (n = 20 coring locations), ingrowth cores (n = 20) and the mini-rhizotron technique (n = 10); elevation, m a.s.l., mean air temperature in °C, annual precipitation in mm year–1, mean soil moisture of mineral
soil in vol%, soil acidity refers to proton concentration in solution from the mineral soil (in mmol l–1), C:N ratio refers to the organic layer. r2 and r2adj refer to linear or simple non–linear regression models. Significant
results are printed in bold (P < 0.05), non-linear relationships are marked by #.


Dependent variable










Soil moisture







Table 9. Correlation analyses between three root production fractions and six climatic and edaphic variables.

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Soil acidity




C:N ratio


Root production in tropical forests


Ing Cor


Elevation (m a.s.l.)


Figure 3. Total root production (BNPP) as the sum of fine,
coarse and large root production, with fine root production estimated by three different methods: Max–Min, sequential coring
using maximum–minimum calculation; Ing Cor, ingrowth core
approach; Minirhiz, mini-rhizotron technique.

about 2900 m, only 300 m below the treeline (Hertel et al.
A causal explanation of the increase in fine root biomass (and also of production) with elevation is limited by
the fact that putative influential environmental factors
such as soil acidity, N shortage, soil hypoxia or the concentration of toxic substances in the soil are themselves
closely interrelated, and are also related to elevation – in
fact, all the variables showed a general increase with elevation (or with decreasing temperature). In the absence of
experimental data at this point, it is only possibly to make
some assumptions about the underlying causes, based on
the results of the correlation analyses.
Increasing N limitation of plant growth with increasing
elevation could be a factor which might explain the
increase in fine root biomass at higher elevations, since
trees have in the past been shown to respond to N shortage
by an increase in root biomass, or at least by increasing
their root to shoot ratio (Vaninnen and Mäkelä 2005). In
our transect, evidence in support of the assumption that
strong N limitation of tree growth at upper montane elevation exists arose from two sources – N fertilisation experiments have shown a stimulation of fine root growth
(Graefe et al. 2008) and microbial activity in the soil
(Maraun et al. 2008), and secondly, the observation that
the C:N ratio in leaves and soil organic matter increases
progressively with elevation (Iost 2007; M. Unger, pers.
Hafkenscheid (2000) has suggested that limitation of
tree growth in montane forests in Jamaica may not only be
caused by reduced nutrient supply at high elevations, but
also by the lower nutrient uptake capacity of fine roots in
the cool and often waterlogged soils. Hafkenscheid found
that low concentrations of inorganic N or high contents of
organic N, Al3+ and H+, were each associated with high
polyphenol concentrations in soil extracts. According to a

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G. Moser et al.

hypothesis advanced by Northup et al. (1995), the complexing of nitrate ions by polyphenols can reduce the loss
of these ions with drainage water from N-deficient soils,
thereby increasing the concentration of dissolved organic
N, but reducing that of NH4+ and NO3–. Thus, elevated
phenolic concentrations in soil water may conserve N, and
can also ameliorate Al3+ toxicity through complexing (Hue
et al. 1986). In general, nitrification in many soils is
reduced at pH values < 5.5, but on the other hand nitrifying
fungi may produce NO3– in acidic soils. Krashevska et al.
(2008) showed for our transect that the microbial community
changed with elevation from being bacteria-dominated at
1000 m to fungal-dominated at 3000 m. Despite the low
pH of the mineral topsoil in all five stands, the nitrate and
ammonium concentrations in Stands 1–3 were quite high
and decreased significantly towards the uppermost stands,
4 and 5 (S. Iost, pers. comm.). It therefore seems unlikely
that low pH was a key factor in limiting nitrification in the
upper section of our transect, and more likely that other
factors such as decreases in litter quality and temperature,
and increasing soil moisture and soil phenol concentrations, were responsible for the decrease in N. It was
assumed by Hafkenscheid (2000) that the large amounts of
phenols in the topsoil water of stunted Jamaican mountain
forests were probably exudates from fine roots rather than
leachates from leaf litter. In our own transect, we found a
more or less constant concentration of soluble phenols in
the leaves (M. Unger, pers. comm.), but an increasing concentration of fine root mass with elevation which may support Hafkenscheid’s hypothesis.
We hypothesise that adverse soil conditions in the
upper montane forests, in particular low N and probable
waterlogging, and possibly also high concentrations of
Al3+ and other toxic cations, may have restricted the nutrient supply, thereby stimulating the trees to enlarge their
fine root system and release significant amounts of
polyphenols through root exudation. Increased production
of secondary metabolites in the root system, together with
high fine root production, which compensates for root
losses in an adverse environment, should represent a notable sink for C and nutrients, which in turn must reduce
above-ground productivity and tree height. In the case of
coarse and large roots, strong winds on exposed ridges and
at high elevations may be an additional factor in southern
Ecuador that shifts C allocation to the root system.
Fine root production measurement in tropical
forests – an assessment of methods
Application of the three methods for estimating fine root
production has, in the past, produced highly divergent
results (Nadelhoffer and Raich 1992; Publicover and Vogt
1993; Fahey et al. 1999; Hertel and Leuschner 2002;
Hendricks et al. 2006). This has been confirmed in our own
study, and supports the need for a critical evaluation when
these are applied to tropical montane forests.
The sequential coring approach. Estimates of fine root
production by soil coring are dependent on accurate periodic

assessment of standing root biomass and in heterogeneous
soil on a sufficiently large number of replicate samples. Difficulties in separating live and dead roots may cause systematic errors. A variety of arguments have been advanced
to explain possible underestimates by sequential coring
(Fahey et al. 1999; Lauenroth 2000; Hertel and Leuschner
2002). These include:

• difficulties in synchronising the sampling dates with

the absolute minimum and maximum of fine root
biomass and necromass within the year;
the simultaneous occurrence of production and mortality (McClaugherty et al. 1982; Aber et al. 1985;
Gower et al. 1992; Publicover and Vogt 1993);
lack of seasonality in fine root biomass and
necromass, especially when the maximum–minimum
method is used;
low estimates of root decomposition rates when using
litter bags, with fresh fine roots being exposed; and
when the maximum–minimum method is used to
estimate root production at highly fertile sites
(Hendricks et al. 1993).

On the other hand, sequential coring approaches may lead
to an over-estimate of fine root production, when (i) fine
root biomass is large, as on sites of low fertility (Singh
et al. 1984; Kurz and Kimmins 1987; Nadelhoffer and Raich
1992; Hendricks et al. 1993), (ii) random errors in biomass
estimates are high, and (iii) a high spatial heterogeneity of
root biomass is linked to weak seasonality. In (iii),
repeated sampling may lead to biomass and necromass
differences that are not significant, and additionally are
confounded by large random errors (Sala et al. 1988;
Lauenroth 2000; Nadelhoffer 2000). Sequential coring
combined with the compartmental flow calculation is particularly sensitive to overestimation under non-seasonal
conditions (Sala et al. 1988).
In the Ecuador transect, underestimation of fine root
production by sequential coring is most likely to have
occurred in the lowermost stands (1050 m and 1540 m elevation), where biomass seasonality was low and where
live fine roots were used in the decomposition experiments
instead of the more realistic dead root material, and likely
to underestimate decomposition rate. Indeed, production
estimates obtained from sequential coring in Stands 1 and 2
were lower than those derived from ingrowth cores. In
contrast, root biomass seasonality was greater in the uppermost stands, thus reducing potential bias caused by this
type of error. However, at 1890, 2380 and 3060 m, fine
root bio- and necromass were high and showed a large
spatial variability (Table 10), in particular when applying
the compartmental flow calculation. The unrealistically high
production estimates for Stands 3 to 5 (>12 Mg ha–1 year–1)
are probably a result of this variation.
Ingrowth core approach. This approach is based on the
assumption that disturbing roots and soil during core installation do not alter root dynamics during the ingrowth period

Root production in tropical forests
Table 10. Mean coefficients of variation (CV = percent standard deviation) to indicate temporal and spatial variability of fine
root mass data (mean coefficients of variation in live and dead
roots) in the five stands during sequential coring campaigns.

Seasonal CV organic
Spatial CV

Stand Stand


Stand Stand






Downloaded At: 09:50 1 December 2010

Season, n = 8; spatial variation, n = 64.

(Lauenroth 2000). The method may lead to overestimates
(i) if the severing of roots during core installation stimulates the proliferation of adventitious roots, (ii) when
chemical and physical properties of the soil have been
altered, thereby promoting root growth, in particular in
experiments with soil substrates other than the local soil,
or (iii) when reduced root competition due to low root
densities in the cores favours root growth (Vogt et al.
1998; Fahey et al. 1999; Lauenroth 2000; Hertel and
Leuschner 2002).
In the Ecuadorian transect, overestimation of fine root
production by the ingrowth core method may have occurred
in Stands 2 and 3, where a proliferation of adventitious
root growth is likely to have occurred after the roots were
relieved from competition in the densely rooted topsoil. In
contrast, alteration of chemical and physical soil properties should have played only a minor role, because local
soil material was used as growing medium.
On the other hand, the ingrowth core approach may
lead to an underestimate of root growth in cases where (i)
the core installation causes a heavy disturbance in the
rhizosphere, (ii) root growth is resumed only after a
considerable delay period and the length of delay cannot
be accurately determined (Vogt et al. 1998), or (iii) root
loss due to decomposition during the experiment is not
allowed for in the analysis (Steele et al. 1997; Lauenroth
2000; Hertel and Leuschner 2002).
If the cores are exposed for fairly long periods, as in
the present study (15 months), the possible confounding
effect of the initial disturbance may be reduced, whereas
errors related to root death and decomposition increase.
Hertel and Leuschner (2002) have proposed the use of
ingrowth cores of small diameter to minimise delay during
the recolonisation process with regrowing fine roots and
reducing the effect of reduced root competition. A large
problem of ingrowth core studies is the unknown length of
the initial delay, since an additional ingrowth core experiment with variable exposure periods can give only approximate estimates of the delay period. We therefore preferred
to apply a uniform delay period of three months in all the
five forest stands. Nevertheless, the delay period at lower
elevations (1050 and 1540 m) was probably shorter,
resulting in an overestimate of the actual root production
rate. On the other hand, the relatively high decomposition
rates in the stands of lower elevation in the transect may


have masked this effect, leading to a significant underestimate of fine root production in Stands 1 and 2. At higher
elevations, with cool soil temperatures and frequent waterlogging, the delay period may have been longer than three
months, causing an underestimation of root production at
2340 and 3060 m.
Mini-rhizotron approach. This technique enables the
direct observation of fine root growth and death in the
rhizosphere. When combined with root biomass determination, this approach may yield more reliable estimates of
fine root production of forests than any other available
technique (Hendricks et al. 2006), particularly in climates
with low seasonality, like Ecuador. The installation of the
rhizotron tubes may represent a similar disturbance to the
rhizosphere as that with the ingrowth core approach. It
requires a recovery period of at least six months before
root initiation and death may have regained a quasi-steady
state again. In cool environments with slower root growth
(e.g. in the present study at 2450 m and 3060 m elevation),
recovery may take even longer (Graefe et al. 2008). Minirhizotron studies along temperature gradients may thus
encounter different recovery periods at the sites being
compared. To counter this, we focused on root length loss
rather than root growth, and related this to mean standing
fine root biomass in calculating root turnover. Even if new
root growth partly represented a compensation for losses
due to the initial disturbance event, root death would
reflect mortality caused by physiological and local environmental factors, thus giving a better estimate of turnover
than calculations based on root growth.
Estimates of fine and coarse root production
With the mini-rhizotron approach, we estimated root
production in the four lowermost stands (1–4) to be 2.3 to
3.7 Mg ha–1 year–1, indicating a significant increase along
the elevation transect when Stand 5 was also taken into
account. However, the very high value obtained for Stand
5 at 3060 m (9.4 Mg ha–1 year–1) may represent an overestimate, for two possible reasons. Firstly, it is unclear if
the root growth and death events observed in the minirhizotron tubes in the uppermost 10 cm of the soil profile
were representative of the entire profile, in particular in
the very thick, acid and moist organic soils of the uppermost stands. It is also questionable if the growth pattern of
the few visible fine roots in the tubes at 3060 m were representative of all roots growing in the uppermost 10 cm of
this soil profile. This type of error should be less severe in
the warmer soils with thinner organic layers at lower elevations, where the number of roots observed was much
higher. Secondly, it is likely that fine root growth would
be slower at higher elevations with lower temperatures,
and this would suggest that longer equilibration periods
should be allowed for the mini-rhizotron tubes after
installation in high-elevation forests (Graefe et al. 2008).
Since we had no data on the duration of the ‘installation
shock’ at different elevations, we used an identical putative
equilibration period (six months) throughout the transect.

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G. Moser et al.

If the linear increase in fine root production observed
between 1050 and 2380 m is extrapolated to the uppermost
stand at 3060 m, a doubling of root production along
2000 m altitude is obtained. We therefore used a conservative extrapolated estimate of fine root production (4.4
Mg ha–1 year–1) and for total BNPP values (5.3 Mg ha–1
year–1) for the 3060 m stand, which fitted well with the
data on estimated canopy C gain and the C balance of the
stands (C. Leuschner, G. Moser and A. Zach, unpublished
For coarse and large root production, the present study
is to our knowledge the first to provide comprehensive
empirical data for a tropical montane forest. Clearly, the
calculation of coarse root production from coarse root
biomass data and diameter increment recorded at 20 root
segments per stand close to the soil surface can give only
an approximate estimate. Since we located the soil pits for
root system analysis at random and avoided the immediate
vicinity of large stems, our data are probably underestimates. Moreover, only roots with diameters between 30
and 320 mm were used for incremental measurement, despite the large range of root diameters present (2 to >> 300
mm). Thus, the data only indicate the magnitude of coarse
and large root production. Furthermore, since coarse and
large root biomass in the stands is at least 4–10 times
greater than fine root biomass, and large roots directly
under the stems (which were not investigated) may possible be more important in low- than in high-elevation
stands, our data may perhaps indicate altitudinal trends in
total root biomass and production which do not exist in
reality. Nevertheless, it is important to point out that the
highest growth rates of large diameter roots were observed
in the most wind-exposed stands, 2 and 5, with a high
demand for tree anchorage and therefore coarse root
growth. Furthermore, coarse and large root production
appeared to be particularly high in the organic layer of
Stand 5, with an extraordinarily high standing biomass of
large diameter roots (38 Mg ha–1).
As mentioned earlier, the three different methods for
fine root production gave highly differing results. While the
production estimates obtained with the three techniques
were quite similar for Stand 1 at 1050 m elevation, large
differences resulting from the three approaches appeared
with increasing elevation. According to the sequential
coring approach, a 10- to 35-fold increase in fine root production (dependent on the method of calculation) occurred
along the slope. The mini-rhizotron data also indicated an
increase in production with increasing elevation, although
fine root production at the uppermost stand was two- to
eightfold lower than that calculated using the sequential
coring approach. The ingrowth core method indicated
highest fine root production at medium elevation, and low
rates at both 1050 m and 3060 m elevation.
Carbohydrate availability for root production
Data on LAI, photosynthetic activity of the trees and irradiance levels in the five stands of the Ecuador transect

(Moser et al. 2007; M. Unger, pers. comm.; B. Wittig,
pers. comm.) suggested that canopy C gain decreased by
about 50% between 1050 m and 3060 m. LAI decreased
by a factor of about 2.7, while photosynthetic capacity per
unit leaf area and incident radiation changed little with elevation. On the other hand, self shading is greater at lower
elevation, suggesting that the decrease in canopy C gain
may be less than deduced from the LAI decrease.
Since above-ground net primary production (stem increment, leaf growth and twig and fruit production) decreased
4.2-fold between 1050 and 3060 m (G. Moser et al.,
unpublished data), which is a greater decrease than the
assumed decline in canopy C gain, we suggest that more
carbohydrates must be available for root growth in the high
elevation stands than at lower altitudes. This is supported by
the observation that above-ground wood respiration greatly
decreases with elevation in this transect (Zach et al. 2008),
leaving more carbohydrates available for below-ground
When applied to the Ecuadorian mountain forest stands,
the three approaches for estimating fine root production
are all affected by more or less serious shortcomings. The
reliability of the data is best assessed by comparing the
root production and turnover figures with independently
derived data from estimated tree C budgets. The C budgets
along the 2000 m elevation transect have led us to reject
the results of the sequential coring approach, which gave
highly unrealistic values for the uppermost stands. The
ingrowth core method showed no clear elevational trend in
fine root production, despite the clear environmental
gradients, and this may therefore also be regarded as an
unsuitable approach. We conclude that the most reliable
results can be expected from the mini-rhizotron approach,
combined with assessment of fine root biomass stocks,
even though in our study a certain over-estimate of root
turnover may occur in the 3060 m stand. The minirhizotron data showed an increase in fine root production
with elevation, at least above 2000 m, that was accompanied by a growing stock of live and dead fine roots. Future
investigations will require additional installation of observation tubes in lower soil horizons in order to quantify
vertical differences in root dynamics in the thick organic
profiles. Coarse and large roots are particularly abundant
and have elevated growth rates at sites with a high demand
for tree anchorage, which is the case at wind-exposed
ridges at higher elevations.
Despite a certain bias in the coarse and large root
production figures, our data indicate that C allocation in
southern Ecuadorian tropical montane forest trees shifts
with increasing elevation from above-ground to belowground organs, since above-ground C sinks decrease and
below-ground sinks increase between 1000 m and 3000 m.
According to the resource balance hypothesis formulated
by Bloom et al. (1985), this conspicuous shift at higher
elevations is best explained by the growing importance of

Root production in tropical forests
soil resource limitation, rather than light limitation of plant
growth, that promotes root rather than shoot growth in montane and upper montane forests.
We would like to thank S. Iost, Technical University of Dresden,
for very fruitful cooperation and for providing data on soil type,
chemistry and soil biological activity, M. Unger (University of
Göttingen) for his data on the polyphenol content of roots and on
radiation, and C. Bertsch (University of Göttingen) for help in
fine root analysis. We also thank P. Emck (University of Erlangen) for the precipitation data. We are grateful to the Fundación
Científica San Francisco (Nature and Culture International) for
permission to work on the ECSF, to the Ministerio del Ambiente
for research permits and to the German Science Foundation
(DFG) for financial funding within the Research Unit 402.

Notes on contributors

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Gerald Moser conducted his Ph.D. research on the above-ground
and below-ground carbon budgets of Ecuadorian mountain forests and is currently a research associate at Giessen University,
Christoph Leuschner is a professor of Plant Ecology at Göttingen
University, Germany, with a research focus on the ecology of
temperate and tropical forests.
Marina Röderstein completed her Ph.D. research on fine root
biomass in Ecuadorian mountain forests.
Sophie Graefe researched fine root dynamics in Ecuadorian forests
for her Ph.D. and currently works as an agricultural research
associate in Colombia.
Nathalie Soethe studied the biomass and growth of large roots in
Ecuadorian mountain forests; she is now a research associate at
the University of Greifswald, Germany.
Dietrich Hertel is a senior scientist in the Department of Plant
Ecology, Göttingen University, with a research focus on tree root

Aber JD, Melillo JM, Nadelhoffer KJ McClaugherty CA, Pastor J.
1985. Fine root turnover in forest ecosystems in relation to
quantity and form of nitrogen availability: a comparison of
two methods. Oecologia 66:317–321.
Bauhus J, Bartsch N. 1996. Fine-root growth in beech (Fagus
sylvatica) forest gaps. Canadian Journal of Forest Research
Bloom AJ, Chapin III FS, Mooney HA. 1985. Resource limitation
in plants – an economic analogy. Annual Review of Ecology
and Systematics 16:363–392.
Clark DA, Brown S, Kicklighter DW, Chambers JQ, Thomlinson
JR, Ni J. 2001a. Measuring net primary production in forests: concepts and field methods. Ecological Applications
Clark DA, Brown S, Kicklighter DW, Chambers JQ, Thomlinson
JR, Ni J, Holland EA. 2001b. Net primary production in
tropical forests: an evaluation and synthesis of existing field
data. Ecological Applications 11:371–384.
Edwards NT, Harris WF. 1977. Carbon cycling in a mixed deciduous forest floor. Ecology 58:431–437.
Fahey TJ, Bledsoe CS, Day FP, Ruess RW, Smucker JM. 1999.
Fine root production and demography. In: Robertson GP,
Bledsoe CS, Coleman C, Sollins P, editors. Soils methods for


long-term ecological research. New York: Oxford University
Press. p. 437–455.
Fahey TJ, Hughes JW, Pu M, Arthur MA. 1988. Root decomposition and nutrient flux following whole-tree harvest of
northern hardwood forest. Forest Science 34:744–768.
Fairley RI, Alexander IJ. 1985. Methods of calculating fine root
production in forests. In: Fitter AH, Atkinson D, Read DJ,
editors. Ecological interactions in soil, plants, microbes and
animals. Oxford: Blackwell. p. 37–42.
Gower ST, Vogt KA, Grier CC. 1992. Carbon dynamics of
Rocky Mountain Douglas-fir – influence of water and nutrient availability. Ecological Monographs 62:43–65.
Graefe S, Hertel D, Leuschner C. 2008. Estimating fine root turnover in tropical forests along an elevational transect using
mini-rhizotrons. Biotropica 40:536–542.
Hafkenscheid RLLJ. 2000. Hydrology and biogeochemistry of
tropical montane rain forests of contrasting stature in the
Blue Mountains, Jamaica. [PhD thesis]. [Amsterdam]
Universiteit Amsterdam.
Hendrick RL, Pregitzer KS. 1992. Spatial variation in tree root
distribution and growth associated with minirhizotrons. Plant
and Soil 143:283–288.
Hendrick RL, Pregitzer KS. 1996. Applications of minirhizotrons
to understand root function in forests and other natural ecosystems. Plant and Soil 185:293–304.
Hendricks JJ, Hendrick RL, Wilson CA, Mitchell RJ, Pecot SD,
Guo DL. 2006. Assessing the patterns and controls of fine
root dynamics: an empirical test and methodological review.
Journal of Ecology 94:40–57.
Hendricks JJ, Nadelhoffer KJ, Aber JD, 1993. Assessing the role
of fine roots in carbon and nutrient cycling. Trends in Ecology
and Evolution 8:174–178.
Hertel D. 1999. Das Feinwurzelsystem von Rein- und Mischbeständen der Rotbuche: Struktur, Dynamik und interspezifische Konkurrenz. Dissertationes Botanicae
Hertel D, Leuschner C. 2002. A comparison of four different fine
root production estimates with ecosystem carbon balance
data in a Fagus–Quercus mixed forest. Plant and Soil 239:
Hertel D, Leuschner C. 2010. Fine root mass and fine root
production in tropical moist forests as dependent on soil,
climate and elevation. In: Bruijnzeel LE, Scatena FH, Hamilton LS, editors. Mountains in the mist: Science for conserving and managing tropical montane cloud forests.
Cambridge: Cambridge University Press.
Hertel D, Leuschner C, Hölscher D. 2003. Size and structure of
fine root system in old-growth and secondary tropical montane
forests (Costa Rica). Biotropica 35:143–153.
Homeier J, Werner FA, Gradstein, SR Breckle S-W & Richter
M. 2008. Potential vegetation and floristic composition of
Andean forests in South Ecuador, with a focus on the RBSF.
In: Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R,
editors. Gradients in a tropical mountain ecosystem of Ecuador. Berlin (Germany): Springer Verlag, (Ecological Studies
198). p. 87–100.
Hue NV, Craddock GR, Adams F. 1986. Effect of organic acids
on aluminum toxicity in subsoils. Soil Science Society of
America Journal 50:28–34.
Iost S. 2007. Soil respiration, microbial respiration and mineralization in soils of montane rainforests of Southern Ecuador:
influence of altitude. [dissertation]. [Dresden, Germany]:
Technical University of Dresden. [accessed 14 September
2009] Available at
Kitayama K, Aiba S-I. 2002. Ecosystem structure and productivity of tropical rain forests along altitudinal gradients with
contrasting soil phosphorus pools on Mount Kinabalu,
Borneo. Journal of Ecology 90:37–51.

Downloaded At: 09:50 1 December 2010


G. Moser et al.

Krashevska V, Bonkowski M, Maraun M, Ruess L, Kandeler E,
Scheu S. 2008. Microorganisms as driving factors for the
community structure of testate amoebae along an altitudinal
transect in tropical mountain rain forests. Soil Biology and
Biochemistry 40:2427–2433.
Kurz WA, Kimmins JP. 1987. Analysis of some sources of error
in methods used to determine fine root production in forest
ecosystems – a simulation approach. Canadian Journal of
Forest Research 17:909–912.
Lauenroth WK. 2000. Methods of estimating below-ground net
primary production. In: Sala OE, Jackson RB, Mooney HA,
Howarth RW, editors. Methods in ecosystem science. New
York: Springer Verlag. p. 58–71.
Leuschner C, Hertel D, Coners H, Büttner V. 2001. Root competition between beech and oak: a hypothesis. Oecologia
126: 276–284.
Majdi H. 1996. Root sampling methods – applications and limitation of the minirhizotron technique. Plant and Soil 185:
Maraun M, Illig J, Sandman D, Krashevskaya V, Norton RA,
Scheu S. 2008. Soil fauna. In: Beck E, Bendix J, Kottke I,
Makeschin F, Mosandl R, editors. Gradients in a tropical
mountain ecosystem of Ecuador. Berlin (Germany): Springer
Verlag (Ecological Studies 198). p.181–192.
McClaugherty CA, Aber JD, Melillo JM. 1982. The role of fine
roots in the organic matter and nitrogen budgets of two forested ecosystems. Ecology 63:1481–1490.
Moser G, Hertel D, Leuschner C. 2007. Altitudinal change in
LAI and stand leaf biomass in tropical montane forests – a
transect study in Ecuador and a pan-tropical meta-analysis.
Ecosystems 10:924–935.
Moser G, Röderstein M, Soethe N, Hertel D, Leuschner C. 2008.
Altitudinal changes in stand structure and biomass allocation
of tropical mountain forests in relation to microclimate and
soil chemistry. In: Beck E, Bendix J, Kottke I, Makeschin F,
Mosandl R, editors. Gradients in a tropical mountain ecosystem of Ecuador. Berlin (Germany): Springer Verlag (Ecological Studies 198). p. 229–242.
Nadelhoffer KJ. 2000. The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New
Phytologist 147:131–139.
Nadelhoffer KJ, Raich JW. 1992. Fine root production estimates
and below-ground carbon allocation in forest ecosystems.
Ecology 73:1139–1147.
Northup RR, Dahlgren RA, Yu ZS. 1995. Intraspecific variation of
conifer phenolic concentration on a marine terrace soil acidity
gradient – a new interpretation. Plant and Soil 171: 255–262.
Persson H. 1978. Root dynamics in a young Scots pine stand in
Central Sweden. Oikos 30:508–519.
Persson H. 1980. Fine-root dynamics in a Scots pine stand with
and without near optimum nutrient and water regimes. Acta
Phytogeographica Suecica 68:101–110.

Powell SW, Day FP. 1991. Root production in four communities
in the great dismal swamp. American Journal of Botany 78:
Publicover DA, Vogt KA. 1993. A comparison of methods for
estimating forest fine root production with respect to sources
of error. Canadian Journal of Forest Research 23:1179–1186.
Raich JW, Russell AE, Vitousek PM. 1997. Primary productivity
and ecosystem development along an elevational gradient on
Mauna Loa, Hawai’i. Ecology 78:707–721.
Richter M, Diertl K-H, Peters T, Bussmann R. 2008. Vegetation
structures and ecological features of the upper timberline
ecotone. In: Beck E, Bendix J, Kottke I, Makeschin F,
Mosandl R, editors. Gradients in a tropical mountain ecosystem of Ecuador. Berlin (Germany): Springer Verlag (Ecological Studies 198). p. 123–135.
Sala OE, Biondini ME, Lauenroth WK. 1988. Bias in estimates
of primary production: an analytical solution. Ecological
Modelling 44:43–55.
Santantonio D, Grace JC. 1987. Estimating fine-root production
and turnover from biomass and decomposition data: a compartment-flow model. Canadian Journal of Forest Research
Singh JS, Lauenroth WK, Hunt HW, Swift DM. 1984. Bias and
random errors in estimators of net root production – a simulation approach. Ecology 65:1760–1764.
Steele SJ, Gower ST, Vogel JG, Normal JM. 1997. Root mass,
net primary production and turnover in aspen, jack pine and
black spruce forests in Saskatchewan and Manitoba, Canada.
Tree Physiology 17:577–587.
Vaninnen P, Mäkelä A. 2005. Carbon budget for Scots pine
trees: effect of size, competition and site fertility on growth
allocation and production. Tree Physiology 25:17–30.
van Praag HJ, Sougnez-Remy S, Weissen F, Carletti G. 1988.
Root turnover in a beech and a spruce stand of the Belgian
Ardennes. Plant and Soil 105:87–103.
Vogt KA, Persson H. 1991. Measuring growth and development
of roots. In: Lassoie JP, Hinckley TM, editors. Techniques
and approaches in forest tree ecophysiology. Florida: CRC
Press. p. 477–501.
Vogt KA, Vogt DJ, Bloomfield J. 1998. Analysis of some direct
and indirect methods for estimation root biomass and production of forests at an ecosystem level. Plant and Soil 200:71–89.
Wang HQ, Hall CAS, Scatena FN, Fetcher N, Wu W. 2003.
Modeling the spatial and temporal variability in climate and
primary productivity across the Luquillo Mountains, Puerto
Rico. Forest Ecology and Management 179:69–94.
Weaver PL, Murphy PG. 1990. Forest structure and productivity in Puerto Rico’s Luquillo Mountains. Biotropica
Zach A, Horna V, Leuschner C. 2008. Elevational changes in
woody tissue CO2 efflux rates in a tropical mountain rainforest in southern Ecuador. Tree Physiology 28:67–74.