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Methods for estimating root biomass and production in forest and woodland
ecosystem carbon studies: A review

Article  in  Forest Ecology and Management · September 2015

DOI: 10.1016/j.foreco.2015.08.015

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 Forest Ecology and Management 359 (2016) 332–351

Contents lists available at ScienceDirect

Forest Ecology and Management

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

Methods for estimating root biomass and production in forest

and woodland ecosystem carbon studies: A review q
Shalom D. Addo-Danso a,b,⇑, Cindy E. Prescott a, Andrew R. Smith c
a
Belowground Ecosystem Group, Department of Forest and Conservation, Faculty of Forestry, University of British Columbia, 2424 Main Mall, Vancouver, BC V6T 1Z4, Canada
b
Ecosystem Services and Climate Change Division, CSIR-Forestry Research Institute of Ghana, P.O. Box UP 63, KNUST, Kumasi, Ghana
c
School of the Environment, Natural Resources, and Geography, Bangor University, Gwynedd LL57 2UW, UK

a r t i c l e i n f o a b s t r a c t

Article history: Fine and coarse roots are key contributors to belowground net primary productivity, and play critical
Received 30 April 2015 roles in the biogeochemical cycling of forest and woodland ecosystems. Despite their critical roles, roots
Received in revised form 11 August 2015 have been understudied mainly due to methodological challenges. There is currently no consensus on
Accepted 13 August 2015
which methods are most suitable to accurately study root biomass and production. Critical evaluation
Available online 9 September 2015
of the assumptions, strengths and inherent limitations of methods to study root biomass and production
are necessary to help investigators decide which method is best for their purposes. This synthesis com-
Keywords:
pares existing methods for root biomass and production estimation based on relevant criteria that
Carbon allocation
Coarse-root production
include cost, labor requirements, time efficiency and accuracy and, also compares fine- and coarse-root
Fine-root biomass biomass and production estimates from different methods measured at the same sites. Root excavation
Ground-Penetrating Radar and soil-pit methods are commonly used to estimate coarse-root biomass, despite the high cost and labor
Ingrowth-core required. Ground-Penetrating Radar is a very promising indirect approach to estimate coarse-root bio-
Soil-pit mass, but may not be suitable for ecosystems with dense understory and soils with high organic matter
and ion contents. Soil-core remains the most preferred method to estimate fine-root biomass. Empirical
models are accepted as fast and cost-effective indirect approach to predict fine- and coarse-root biomass
and production. Fine-root production is usually estimated with the (mini) rhizotrons, sequential-coring
and ingrowth-core methods. Coarse-root biomass estimates were not significantly different between
soil-pit and soil-core methods. There was a significant positive correlation (r2 = 0.91, p < 0.0001) between
fine-root biomass estimates obtained from soil-pit and soil-core methods. Fine-root production estimates
were lower in the ingrowth-core (2.06 ± 0.23 Mg ha!1 year!1) compared to the (mini) rhizotrons
(3.81 ± 0.46 Mg ha!1 year!1) and sequential-coring (3.84 ± 0.93 Mg ha!1 year!1) methods. Based on the
reviewed literature and comparative analysis we propose that (mini) rhizotrons should be preferred
over the others in estimating fine-root production. In situations where cost and site conditions preclude
their use, the sequential-coring and ingrowth-core methods are suitable. The ingrowth-core should be
used with caution in sites where root growth is slow and root biomass may be influenced by strong
seasonal fluctuations. Multiple methods are still recommended for yielding realistic estimates of fine-
and coarse-root production, and more comparative studies of different methods should be conducted
on the same sites.
! 2015 Elsevier B.V. All rights reserved.

1. Introduction
Fine and coarse roots are major contributors to the total bio-
mass pools of forest and woodland ecosystems, and play critical
q
This article is part of a special section entitled ‘‘Forests, Roots and Soil Carbon”.
⇑ Corresponding author at: Belowground Ecosystem Group, Department of Forest
and Conservation, Faculty of Forestry, University of British Columbia, 2424 Main
Mall, Vancouver, BC V6T 1Z4, Canada.
E-mail address: shalomdanso@hotmail.com (S.D. Addo-Danso).
roles in the cycling and allocation of carbon (C) and nutrients
(Clark et al., 2001; Brunner and Godbold, 2007; Malhi et al.,
2011; Smyth et al., 2013; Raich et al., 2014). A significant fraction
of C assimilated by plants through photosynthesis is transferred to
roots and their symbionts (Litton et al., 2007; McCormack et al.,
2015); this may even exceed the amount allocated to aboveground
components (e.g. Moser et al., 2011). The carbon transferred
belowground is estimated to account for 22–63% of the total gross
primary productivity of forests (Litton et al., 2007). This large flux
of C exerts a profound influence on the regulation of major soil

http://dx.doi.org/10.1016/j.foreco.2015.08.015
0378-1127/! 2015 Elsevier B.V. All rights reserved.
 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351
processes that affect productivity and biogeochemical cycling in
these ecosystems (Prescott, 2010; Clemmensen et al., 2013; Raich
et al., 2014; Zhang and Wang, 2015). Despite these critical roles,
roots have been understudied, and are poorly represented in many
process-based ecosystem models, limiting the models ability to
predict ecosystem responses to environmental changes and man-
agement practices (Smithwick et al., 2014; Warren et al., 2015).
The uncertainty about root dynamics also hampers efforts to accu-
rately estimate pool size for C accounting and climate mitigation
measures such as the Reduced Emissions from Deforestation and
Forest Degradation (REDD+) (Smyth et al., 2013; Yuen et al.,
2013). This knowledge gap is partly attributable to methodological
challenges in sampling roots to estimate biomass production and
turnover (Vogt et al., 1998; Bledsoe et al., 1999; Makkonen and
Helmisaari, 1999).
Estimation of fine and coarse root biomass and production can
be grouped into direct and indirect methods. Fine-root biomass
and production have been estimated with direct methods that
include soil-core/sequential-coring (Makkonen and Helmisaari,
1999; Lauenroth, 2000), monolith (Bledsoe et al., 1999; Makita
et al., 2011), soil-pit (Millikin and Bledsoe, 1999; Park et al.,
2007), ingrowth-core (Persson, 1979; Vogt et al., 1998) and (mini)
rhizotrons (Taylor et al., 1990; Madji, 1996), and indirectly through
the use of empirical models (Shinozaki et al., 1964b; Kurz et al.,
1996). For coarse roots, direct methods include root excavation
(Bledsoe et al., 1999; Niiyama et al., 2010), soil-pit/soil-pit
ingrowth (Lawson et al., 1970; Kangas, 1992), wall or trench pro-
files and soil-core (van Noordwijk et al., 2000; Achat et al., 2008;
Major et al., 2012), while the indirect methods include, but are
not limited to, size-mass allometric equations (Whittaker et al.,
1974; Kenzo et al., 2009; Brassard et al., 2011a), root–shoot or
belowground–aboveground ratio (Keith et al., 2000; Levigne and
Krasowski, 2007; Malhi et al., 2009), Ground-Penetrating Radar
(GPR) (Butnor et al., 2001; Samuelson et al., 2015), and root bio-
mass increment or difference (Steele et al., 1997; Kajimoto et al.,
1999) as well as root radial increment (Zach et al., 2010; Moser
et al., 2011).
There is no consensus in the literature on how best to estimate
root biomass, production and turnover (Vogt et al., 1998; Bledsoe
et al., 1999; Levillain et al., 2011; Milchunas, 2012; Yuan and
Chen, 2012a). For instance, in a global study that compared fine
root production estimates for terrestrial ecosystems, Yuan and
Chen (2012a) reported significantly higher fine-root production
estimates from indirect than direct methods, which is contrary to
other studies where no differences between direct and indirect
methods were observed (e.g. Vogt et al., 1998; Finér et al., 2011).
This uncertainty means that the choice of a method may be deter-
mined by considerations such as cost, labor availability, site con-
straints and individual preferences rather than accuracy and
precision (Vogt et al., 1998; Levillain et al., 2011; Makita et al.,
2011), with implications for modeling ecosystem C budget and
allocation patterns. This lack of consensus therefore calls for criti-
cal evaluation of the assumptions, strengths and inherent limita-
tions of the various methods to help investigators decide which
method is best for their purposes.
It is often recommended to use multiple methods to quantify
root dynamics (Vogt et al., 1998; Hendricks et al., 2006; Yuan
and Chen, 2012a), but few studies compare methods at the same
sites and at the same sampling time (e.g. Makkonen and
Helmisaari, 1999; Hertel and Leuschner, 2002; Ostonen et al.,
2005; Hendricks et al., 2006; Moser et al., 2010; Levillain
et al., 2011; Girardin et al., 2013; Yuan and Chen, 2012a; Sun
et al., 2015). This study builds on earlier reviews (e.g. Vogt et al.,
1998), but with greater emphasis on coarse roots due to the pre-
sent recognition of their important roles in ecosystem C budgets
and allocation patterns (Clark et al., 2001; Smyth et al., 2013;
333
Doughty et al., 2014; Varik et al., 2015; Zhang and Wang, 2015).
The objectives of this review were to (1) synthesize and compare
existing methods for root biomass and production based on rele-
vant criteria, and (2) compare fine and coarse root biomass and
production estimates from different methods measured at the
same sites.
2. Methods
2.1. Literature search and data compilation
Data was compiled through a literature search from journal
platforms (Web of Science, Scirus, JSTOR and Google Scholar) and
library sources using keywords and the terms ‘fine root’, ‘coarse
root’, ‘root biomass and production’ and ‘belowground biomass
allocation’. All data are from studies conducted in forest and wood-
land ecosystems (as they contain more than 60% of terrestrial C
(Dixon et al., 1994)), which should improve the clarity of the rela-
tionship between root biomass and production estimates provided
by different methods. Stands of all ages were used, including man-
aged (irrigated, thinned and fertilized) and unmanaged stands.
With respect to root sampling, additional criteria were: (i) the
study must have included the diameter used to define fine and
coarse roots; (ii) roots were sampled by using the soil-pit and
soil-core methods to quantify biomass; (iii) fine-roots were sam-
pled using at least two of the direct methods (ingrowth-core,
(mini) rhizotrons and sequential-coring) to estimate production;
(iv) sampling for fine-root production should have lasted at least
one vegetation season or 12 months; and (v) data were collected
from a single site and within the same period.
Criteria used to identify fine and coarse roots are not uniform,
and are usually defined based on arbitrary diameter classes (e.g.
Nadelhoffer and Raich, 1992; Resh et al., 2003; Levigne and
Krasowski, 2007; Finér et al., 2011). From the database, fine roots
were defined as 60.5 mm, 61 mm, 62 mm and 65 mm in diame-
ter. Coarse roots also ranged from >2 mm to >50 mm in diameter.
However the majority of the studies defined fine and coarse roots
as 62 mm and >2 mm in diameter (see Appendices A and B and ref-
erences therein). These definitions will be used to broadly classify
fine and coarse roots in the first part of this review. These classifi-
cations have also been used in other reviews (e.g. Yuan and Chen,
2012a; Zhang and Wang, 2015). In the analysis of root biomass and
production, fine and coarse roots were not standardized to specific
diameter classes (Finér et al., 2011), but were considered to be as
defined in the original studies (Nadelhoffer and Raich, 1992).
For the first objective, the database was critically assessed to
extract information on existing root biomass and production meth-
ods (including new and less known ones), their operational princi-
ples and strengths and limitations. From the information gathered
a matrix was developed to compare methods based on criteria such
as ease of field application, cost-effectiveness, labor requirements,
time efficiency, accuracy and impact on the ecosystem (Tables 1
and 2). For this review, time efficiency is considered to be the
person-hours required to complete field (set-up and sampling)
and laboratory processing (Levillain et al., 2011), and accuracy is
the capacity for a method to provide accurate estimates. For the
second objective, root biomass data were compiled from studies
that compared more than one method at the same site. For fine
and coarse roots biomass data were compared for the soil-pit
and soil-core methods. Nine observations were obtained for fine
root biomass, while eleven observations of coarse root biomass
were made from seven studies (Appendix A). The Voronoi trench
was considered as a ‘soil pit’ since its field application is similar
to the soil-pit method (Levillain et al., 2011). Moreover the study
by Levillain et al. (2011) did not compared coarse root biomass
(>10 cm in diameter) between soil pit and soil cores, but was done
 334
Table 1
Comparison of methods for estimating coarse-root biomass and production using selected criteria.

Method Type Operational principle Requirements for optimum Ease of field Cost Labor requirements Time Accuracy Impact on
accuracy application effectiveness efficiency ecosystem
Coarse-root biomass
Root excavation Direct Relates root biomass to aboveground Correction for lost and Difficult-not Costly Laborious Inefficient High Destructive
parameters e.g. DBH broken roots feasible in
many sites

S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351
Soil-pit Direct Assumes roots are uniformly distributed Soil pits must be deep Difficult Costly Laborious Inefficient High Destructive
in pits enough to recover about
90% of roots
Wall or soil trench profile Direct Assumes a positive relationship between Correction for relative root Simple Economical Less labor Efficient Low Non-destructive
counted roots and root length density biomass estimates
produced
Soil-core Direct Equates root biomass to roots in a soil Large diameter corer/auger Simple Costly Laborious Inefficient Low Destructive
column preferably (>10 cm) must
be used
Mass-size allometric equations Indirect Woody components both above-and Validation of models for Simple Economical Less labor Efficient Low Non-destructive
belowground are related in size and age specific sites
Root-shoot or below ground– Indirect Assumes a significant relationship Generation of site-specific Simple Economical Less labor Efficient Low Non-destructive
aboveground ratio between root biomass and aboveground ratios
biomass
Ground-Penetrating Radar (GPR) Indirect Based on geophysical close range remote Well drained sandy soil, Simple-but Costly Less labor Efficient Low Non-destructive
sensing technique with low organic matter usually site
and ion content specific
Coarse-root production
Soil ingrowth pit Direct Assumes production to be proportional More pits required to Difficult Costly Laborious Inefficient High Destructive
to root biomass accumulated in pits over capture root growth and
a period of time distribution
Root biomass increment/difference Direct/ Based on changes in root biomass over a Site-specific models to Simple Depending Laborious or simple- Could be High Destructive or not
Indirect period estimate biomass on approach based on preferred efficient based on preferred
difference approach or not approach
Fraction/percentage of wood Indirect Assumes a general positive relationship Accurate measurement of Simple Economical No labor Efficient Low Non-destructive
production between coarse-root and woody biomass wood parameters e.g.
diameter
Root radial increment Direct Direct measurements of root radial Capture of small coarse- Simple Economical Less labor Efficient Low Non-destructive
growth roots
 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351 335

for medium roots (2–10 cm). Therefore the values produced by the
two methods for the medium roots were used in the analysis.

Non-destructive
Non-destructive

Non-destructive
For fine root production, 58 observations were from studies
comparing ingrowth-core and sequential-coring, while 25 observa-

Destructive

Destructive

Destructive

Destructive

Destructive

Destructive
ecosystem
Impact on

tions were from comparative studies of ingrowth-core and (mini)

rhizotrons. There were 11 observations from studies that com-
pared sequential-coring and (mini) rhizotron methods (Appendix
B). A total of 28 studies were considered for fine root production.
Accuracy

Data for (mini) rhizotrons were compiled from studies that used
High

High

High

High
Low
Low

Low

Low

Low
both the minirhizotron and rhizotron to sample roots (e.g. Fahey
and Hughes, 1994; Steele et al., 1997; Metcalfe et al., 2007a;
Inefficient

Inefficient

Inefficient

Inefficient
efficiency

Efficient
Efficient

Efficient

Efficient

Efficient
Girardin et al., 2013). Root biomass or production estimate from
Time

each site was considered as a single observation, even if methods

were compared at different sites (Nadelhoffer and Raich, 1992;
requirements

Finér et al., 2011). In studies where data for forest floor and mineral
Less labor
Less labor

Less labor

Less labor

Less labor
soil were presented separately, they were combined to produce a
Laborious

Laborious

Laborious

Laborious
single value.
Labor

Data from multiple years were averaged. Several approaches

have been developed to convert root-growth data from (mini) rhi-
effectiveness

Economical
Economical

Economical

Economical

zotrons into biomass (Taylor et al., 1990; Metcalfe et al., 2007a;

Milchunas, 2012), and to convert sequential-coring and
Costly

Costly

Costly

Costly

Costly

ingrowth-core data into fine root production estimates

Cost

(Nadelhoffer and Raich, 1992; Vogt et al., 1998; Hendricks et al.,

2006; Brunner et al., 2013). In situations where data were pre-
Ease of field

sented for different approaches within the same method, the aver-
application

age value was used (e.g. Hertel and Leuschner, 2002; Hendricks
Difficult

Difficult
Simple

Simple

Simple
Simple

Simple

Simple

Simple

et al., 2006; Metcalfe et al., 2007a). In a few cases where a range

was given, the average was calculated between the lower and
upper values (e.g. Noguchi et al., 2007).
Large diameter corer/auger preferably (>10 cm)

N inputs, pools and fluxes must be determined

Time and magnitude of root growth for sites

Shorten observational intervals and position

Intervals between sampling dates must be

Good balance between monolith size and

2.2. Statistical analyses

Validation of models for specific sites
Requirements for optimum accuracy

The data extracted were subsequently used to calculate average

fine and coarse root biomass and fine root production estimates for
tubes or plastic frames well

the different methods. The difference between the average esti-

mates among fine and coarse root biomass and fine root produc-
Validation of model

tion methods was tested by student t-test and one-way analysis

should be known
Refer to Table 1

of variance. Regression analysis was used to evaluate correlations

must be used
Comparison of methods for estimating fine-root biomass and production using selected criteria.

between fine root biomass estimates from soil-pit and soil-core

accurately
shortened
number

methods, and fine root production estimates from sequential-

coring and ingrowth-core, ingrowth-core and (mini) rhizotrons,
as well as sequential-coring and (mini) rhizotrons methods. Root
Equates root biomass to roots in a soil column

Assumes root biomass is proportional to roots

Assumes that disturbances to roots and soil do

Images are captured, and converted to biomass

Assumes root production and mortality occur

biomass and production data were converted to Mg ha!1 and

Based on the pipe-model theory of tree form

Assumes that fine-root production is largely

Mg ha!1 year!1 (Yuan and Chen, 2012a), and log-transformed prior

to analysis when necessary. All analyses were performed with the
GraphPad Prism 6 (GraphPad Software, Inc., California, USA) soft-
ware package, with the significance level of p < 0.05.
in soil block or monolith

not affect root ingrowth

3. Results and discussion

Operational principle

driven by soil N
Refer to Table 1

Refer to Table 1

asynchronously

3.1. Literature review

production

3.1.1. Coarse-root biomass and production

Due to their large size and spatial heterogeneity, coarse roots
(mostly >2 mm in diameter) can be difficult and expensive to
quantify in the field. Studies have relied on both direct and indirect
Indirect
Indirect

Indirect
Direct

Direct

Direct

Direct

Direct
Direct

methods to estimate coarse root biomass and production.

Type

Fine-root production
Allometric models

Sequential-coring
(Mini) rhizotrons
Fine-root biomass

3.1.1.1. Direct methods. Coarse roots can be estimated by using

Ingrowth-core

direct methods such as root excavation, soil-pit/soil-pit ingrowth,

Pipe model

wall or trench profiles and soil coring. These methods generally

N budget
Monolith
Soil-core
Method

Soil-pit

produce reliable root-biomass estimates, but have strengths and

Table 2

limitations (Table 1). Therefore investigators should consider

factors such as field adaptability, cost effectiveness, labor
336 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351
requirements, and accuracy as well as their impacts of ecosystems
(Table 1) before selecting a method.
3.1.1.1.1. Root excavation. The root-excavation method has
been used to estimate coarse root biomass (CRB) of individual trees
and stands in tropical (e.g. Misra et al., 1998; Niiyama et al., 2010;
Ryan et al., 2011; Lima et al., 2012), temperate and boreal forest
and woodland ecosystems (e.g. Bledsoe et al., 1999; Millikin and
Bledsoe, 1999; Resh et al., 2003; Ouimet et al., 2008; Brassard
et al., 2011a). The excavation method can generally be distin-
guished into two types, total root and root-ball excavation. With
total root excavation, the entire root system of an individual tree
within a designated radius is excavated manually (Bledsoe et al.,
1999; Berhongaray et al., 2015) or with the help of machinery such
as a tractor, backhoe or power shovel (Brassard et al., 2011a; Ryan
et al., 2011; Fortier et al., 2015). The root-biomass estimates of
individual trees can be related to aboveground biometric parame-
ters such as diameter at breast height (DBH) to develop allometric
equations, which can then be used to estimate belowground
biomass of an entire stand (e.g. Haynes and Gower, 1995; Resh
et al., 2003; Berhongaray et al., 2015). In root-ball excavation, a soil
monolith is centered on the stump of a target tree (Bledsoe et al.,
1999), and the roots (including lateral roots) are recovered follow-
ing soil excavation either manually or mechanically, without
removing the stump. Roots are then washed, dried and weighed
as described above. Although root-ball excavation is considered
an expeditious and cost-effective method to estimate CRB (Miller
et al., 2006), field application has mostly been limited to young
plantations (e.g. Misra et al., 1998; Resh et al., 2003; Miller et al.,
2006).
The main advantage of the excavation method is that it allows
for direct harvesting of coarse roots concentrated mostly around
the base of the stem (Bledsoe et al., 1999; Macinnis-Ng et al.,
2010, resulting in an improved estimate of root biomass (Millikin
and Bledsoe, 1999; Resh et al., 2003). For instance, in a Quercus
douglasii stand in California, Millikin and Bledsoe (1999) reported
higher CRB estimates using the excavation method compared to
soil-pit and soil-core methods, and so recommended the excava-
tion method for estimating CRB. Excavation is considered the only
method that will accurately quantify CRB in individual trees and
whole stands (e.g. Snowdon et al., 2002; Cole and Ewel, 2006;
Ouimet et al., 2008; Niiyama et al., 2010; Ryan et al., 2011), and
is particularly recommended for sites with high spatial hetero-
geneity of roots (Resh et al., 2003).
However, the excavation method can be laborious and expen-
sive (Danjon and Reubens, 2008). According to Danjon et al.
(2005), it could take a whole day for five people to manually uproot
twenty-four 50-year-old Pinus pinaster roots in a sandy spodosol
soil, which is relatively well suited for excavation. The excavation
method may result in sampling error as roots become broken or
lost during excavation (Millikin and Bledsoe, 1999; Niiyama
et al., 2010). Even under ideal conditions complete recovery of
entire root systems is difficult, especially for large trees which usu-
ally have extensive and deep root systems (Bledsoe et al., 1999).
Indeed in a tropical primary forest in Malaysia, Niiyama et al.
(2010) estimated biomass of lost roots to be ca. 19 Mg ha!1,
accounting for 23% of the total CRB. Procedures for determining
the biomass of broken lateral roots from intact laterals or harvest-
ing of broken root fragments following stump excavation have
been developed to correct for lost and broken roots (Santantonio
et al., 1977; Millikin and Bledsoe, 1999; Niiyama et al., 2010;
Brassard et al., 2011a). Excavation is also destructive (Danjon and
Reubens, 2008), as excavation and tree root removal can seriously
disturb soil a long distance from the target tree (Bledsoe et al.,
1999; Cole and Ewel, 2006), and so may not be feasible if minimiz-
ing site disturbance is a priority.
3.1.1.1.2. Soil-pit/soil-pit ingrowth. Soil-pit determination of
root biomass is another direct method frequently used to estimate
coarse root biomass and production (e.g. Kimmins and Hawkes,
1978; Fahey et al., 1988; Eamus et al., 2002; Rau et al., 2009;
Smith et al., 2013; Costa et al., 2014). Soil pits have also been
employed to determine lateral-root distribution in ecosystems
(Bledsoe et al., 1999). With this method a number of trenches are
excavated manually or mechanically, and the soil is collected and
processed to estimate root biomass (Levillain et al., 2011). These
biomass estimates can subsequently be used to establish allomet-
ric relationships with aboveground biometric parameters such as
DBH and basal area to estimate total stand root biomass (Park
et al., 2007). Studies have used varying pit dimensions and layouts,
which typically depend on the size and spatial distribution of
coarse roots (e.g. Rau et al., 2009; Chidumayo, 2014; Costa et al.,
2014); greater numbers of pits being necessary at sites of high
belowground heterogeneity (Bledsoe et al., 1999). A critical aspect
of this method is ensuring that soil pits are excavated deep enough
to recover more than 90% of the roots (Bledsoe et al., 1999). The
sampling depth can be determined in a pilot trial to establish the
maximum rooting depth. For instance, Park et al. (2007) reported
that a sampling depth ranging from 0.95 m to 1.7 m reflected the
natural variation in maximum root depth in mixed deciduous
stands in New Hampshire, US. The soil-pit method can also be used
to quantify coarse root production by removing roots from a vol-
ume of soil, and monitoring the regrowth of roots over a period
of time (Jordan and Escalante, 1980; Kangas, 1992; Lauenroth,
2000). Root production is assumed to be the amount of root bio-
mass accumulated during the interval (Kangas, 1992). The basic
principle behind the soil-pit ingrowth method is similar to the
ingrowth-core method (discussed under Section 3.1.2.1.3), even
though no mesh bag is installed.
The soil-pit method has been found to provide good estimates
of CRB (e.g. Millikin and Bledsoe, 1999; Jackson et al., 2009;
Levillain et al., 2011; Smith et al., 2013). In a Eucalyptus plantation
in Congo, Levillain et al. (2011) found a higher CRB estimate using
the soil-pit method than using soil monoliths. Smith et al. (2013)
also found higher CRB estimates from the soil-pit method com-
pared to the soil-core method in an elevated-CO2 Betula pendula
stand in the UK. However, they also reported lower CRB from soil
pits compared to the soil cores in an elevated-CO2 mixed stand
of Alnus glutinosa, B. pendula and Fagus sylvatica (Smith et al.,
2013). The soil-pit method allows roots to be collected throughout
the soil profile (Park et al., 2007), and therefore deeper roots are
included in the root-biomass estimates (Rau et al., 2009). A large
area is often sampled in each pit (relative to coring methods),
which may improve accuracy of root biomass assessments in
ecosystems with greater heterogeneity of coarse roots (Macinnis-
Ng et al., 2010).
To reduce the labor required to sample coarse roots, CRB is
sometimes estimated from subsamples of soil from soil-pits. This
assumes uniform distribution of roots within pits (Rau et al.,
2009), which may not be a valid assumption (Park et al., 2007).
Nevertheless, because of the general reliability of the soil-pit
method, it is often employed to validate the accuracy of root-
biomass estimates provided by other methods (e.g. Park et al.,
2007; Smith et al., 2013). For example, Smith et al. (2013) used a
CRB estimate determined from soil pits to confirm the validity of
data obtained through soil coring, and found a strong correlation
between the two methods. Soil pits are also considered the best
method for sampling roots in sites with stony soils where stones
can hinder the ability to extract cores from soil and increase root
heterogeneity and sampling bias (Park et al., 2007; Rau et al.,
2009). While the soil-pit method is excellent for sites of high spa-
tial variability of roots, it is also recommended for ecosystems with
low root heterogeneity (Bledsoe et al., 1999).
 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351
Despite its wide use, the soil-pit method has been shown to
under-estimate CRB (e.g. Bledsoe et al., 1999; Park et al., 2007;
Rau et al., 2009; Chidumayo, 2014) probably due to the exclusion
of soil close to tree stems (Park et al., 2007) where coarse-root den-
sity is high. Soil-pit sampling also mostly excludes taproots, root
crowns and lignotubers, thereby under-estimating the total bio-
mass of coarse roots (e.g. Fahey et al., 1988; Millikin and Bledsoe,
1999; Park et al., 2007). Due to the destructive nature of soil pits,
it is not considered to be suitable for directly sampling root bio-
mass of individual trees (Rau et al., 2009), or for the estimation
of coarse root production by soil-pit ingrowth (Jordan and
Escalante, 1980; Kangas, 1992).
3.1.1.1.3. Wall or soil trench profile. The wall or soil-trench
profile is another direct method used to estimate CRB (Epron
et al., 1999; van Noordwijk et al., 2000; Achat et al., 2008). Wall
or trench profiling involves digging a trench with a spade or exca-
vator in a stand to expose the coarse roots. The soil surface is
shaved and flattened to improve root observation (Achat et al.,
2008), and a grid frame is installed onto the trench wall, usually
with nails, down to a specified depth (Grant et al., 2012). Roots that
are exposed along the vertical plane are carefully counted and
mapped (Maurice et al., 2010). Wall profiles can also be pho-
tographed, and the images assembled to map the soil profile
(Schmid and Kazda, 2002). Roots can be traced or images digitised
to determine root length and other root metrics (e.g. number of
tips, forks, etc.) using image analysis software (Schmid and
Kazda, 2002; Lobet et al., 2013). Root length can then be converted
to root biomass per unit area (Metcalfe et al., 2007a). Alternatively,
root biomass may be estimated from root volume data (e.g. Epron
et al., 1999; Curt et al., 2001). The wall profile assumes a positive
relationship between the number of roots on the soil vertical plane,
and the root length density inside the soil column (Bledsoe et al.,
1999). This method is less time-consuming than other direct meth-
ods and is non-destructive, and therefore provides the opportunity
for investigators to quantify root systems in situ over large time
scales (Curt et al., 2001). Curt et al. (2001) noted that observation
and counting of 74 root profiles required about 30 person-days,
compared to the 100 person-days required to completely excavate
one mature tree. Root recordings yet to be converted to biomass
can also be combined with root mass data obtained from other
methods to produce a better estimate of CRB (e.g. Epron et al.,
1999; Achat et al., 2008). For example, Achat et al. (2008) used
the intersection of roots obtained from wall profiles to improve
root biomass estimates from soil-cores for a P. pinaster stand in
south-western France.
The wall profile method is, however, rarely applied, because it
can substantially under-estimate CRB since the relative values pro-
duced have to be corrected (Bledsoe et al., 1999; Levillain et al.,
2011), and therefore its use for estimating CRB has been discour-
aged. Furthermore, when using the wall profile method, soil prop-
erties must be considered in order to visualize undisturbed root
growth. It may also be difficult to distinguish live and dead roots,
and to identify roots of different species (van Noordwijk et al.,
2000; Curt et al., 2001). Although not well suited for estimating
CRB (Bledsoe et al., 1999), the wall profile method is highly recom-
mended for studies of root morphology and density distribution (e.g.
Schmid and Kazda, 2002; Maurice et al., 2010; Grant et al., 2012).
3.1.1.1.4. Soil-core. Soil cores are also used to estimate CRB,
although they may under-estimate CRB (e.g. Millikin and Bledsoe,
1999; Resh et al., 2003; Jackson et al., 2009; Major et al., 2012),
as a result of the small volume of soil sampled (Levillain et al.,
2011), and the infrequent encountering of large roots during coring
(Butnor et al., 2012; Taylor et al., 2013). For instance, in a Eucalyp-
tus plantation in Tasmania, Resh et al. (2003) found that soil cores
under-estimated CRB by 9% compared to estimates from total-tree
excavation. Jackson et al. (2009) also found that increasing CRB in
337
response to CO2 enrichment was only detected when they shifted
from the use of soil cores to soil pits at the Duke FACE experiment
site in Durham, US. On the other hand, Rau et al. (2009) and Smith
et al. (2013) reported no significant difference in CRB estimates
collected using soil-pit and soil-core methods. Resh et al. (2003)
argued that soil-coring is a pragmatic method, as the accuracy is
not usually affected by increasing sampling intensity, and it also
allows for examination of the spatial distribution of coarse roots
both vertically and laterally. It is also simpler, as sampling pro-
cesses and data calculations are considerably less complicated than
either the soil-pit or excavation method (Rau et al., 2009). The cor-
ing device can also be easily transported, and therefore the soil-
core method is efficient for sampling roots in remote sites where
accessibility by heavy-duty equipment is limited (Rau et al., 2009).
3.1.1.2. Indirect methods. Due to the cost and labor requirements of
direct methods for estimating root biomass (Table 1), many inves-
tigators have employed indirect techniques to estimate CRB and
production. These indirect techniques include size-mass allometric
equations, root–shoot or belowground–aboveground ratio, GPR,
root biomass increment or difference, fraction or percentage of
wood production, and root radial increment. The aforementioned
methods are increasingly being applied in field studies because
they provide quick and non-destructive means to quantify the con-
tributions of fine and coarse roots to total forest and woodland bio-
mass and carbon storage.
3.1.1.2.1. Size-mass allometric equations. The size-mass allomet-
ric technique is the most common indirect way to estimate CRB (e.g.
Whittaker et al., 1974; Bledsoe et al., 1999; Návar, 2009; Niiyama
et al., 2010). To develop allometric equations, CRB is usually related
to aboveground parameters like DBH or height (Snowdon et al.,
2002; Brassard et al., 2011a). The basis for these equations is the
assumption that coarse roots grow at a rate which is similar to
wood biomass, and therefore the two components are related in
size and age (Niiyama et al., 2010). Despite some exceptions (e.g.
Bolte et al., 2004; Hunziker et al., 2014), the allometric relation-
ships between wood biomass and CRB in many species are gener-
ally consistent (e.g. Whittaker et al., 1974; Jenkins et al., 2003;
Kenzo et al., 2009; Návar, 2009), and it has been suggested that
CRB in different sites and geographic regions could be estimated
with published allometric equations developed from DBH (e.g.
Brassard et al., 2011a). Different site- and species-specific equa-
tions, as well as generalized equations have been developed, and
applied to estimate CRB in different regions of the world (e.g.
Whittaker et al., 1974; Návar, 2009; Niiyama et al., 2010;
Chidumayo, 2014). For instance, the allometric equations devel-
oped by Whittaker et al. (1974) for broadleaved-deciduous forest
stands in New Hampshire have been used extensively to predict
CRB in northern hardwood tree species such as Acer saccharum
and Fagus grandifolia in the US (Jenkins et al., 2003;
Vadeboncoeur et al., 2007). Allometric equations are useful
because they offer a cost-effective and reliable means to estimate
stand-level CRB (Bledsoe et al., 1999; Xiao et al., 2003;
Vadeboncoeur et al., 2007). Vadeboncoeur et al. (2007) reported that
allometric equations developed to estimate CRB in F. grandifolia,
A. saccharum and Betula alleghaniensis agreed well with root mass
estimated from soil pits. Coarse root allometric equations are also
useful for evaluating temporal changes in root biomass and carbon
stocks in forest ecosystems (Mokany et al., 2006; Niiyama et al.,
2010).
Despite general acceptance, allometric equations may under- or
over-estimate root biomass (Park et al., 2007; Kenzo et al., 2009;
Brassard et al., 2011a). Park et al. (2007) reported a 32% lower
CRB estimate from allometric equations than from soil pits in
young hardwood stands in New Hampshire. Brassard et al.
(2011a) also recorded large variations in Abies balsamea CRB using
338 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351
their own developed models and other allometric models from the
literature. According to Niiyama et al. (2010) the accuracy and pre-
cision of root-biomass estimates are influenced by both the quan-
tity and quality of data used for developing the allometric models.
Some allometric equations do not correct for roots that are lost or
broken during sampling, and this introduces uncertainty when
applied at different sites. Larger trees are also sometimes excluded
during the collection of data used to develop allometric models
affecting the accuracy of extrapolated biomass estimates (Xiao
et al., 2003). Most coarse root allometric equations are not vali-
dated at sites against multiple methods of determining CRB which
would increase accuracy when applied over large spatial scales
(Bolte et al., 2004; Vadeboncoeur et al., 2007).
3.1.1.2.2. Root–shoot or belowground–aboveground ratio. The
root–shoot ratio (RSR) or belowground–aboveground (BG/AG) bio-
mass ratio is a common approach for estimating CRB. The ratio
expresses a general relationship between root biomass and shoot
biomass (Sanquetta et al., 2011; Luo et al., 2012; Poorter and
Sack, 2012; Smyth et al., 2013), which reflects the net effects of car-
bon allocation in a particular ecosystem (Mokany et al., 2006). CRB
is estimated from aboveground biometric parameters such as DBH
and biomass (Levigne and Krasowski, 2007; Malhi et al., 2009),
based on the assumption of a positive relationship between root
biomass and wood biomass (Eamus et al., 2002; Sanquetta et al.,
2011; Poorter and Sack, 2012), which may not hold for all ecosys-
tems (e.g. Barton and Montagu, 2006). Generalized and group-
specific RSR exist for different tree species, forest and woodland
types and biomes (Cairns et al., 1997; IPCC, 2006; Malhi et al.,
2009; Luo et al., 2012; Smyth et al., 2013; Yuen et al., 2013). A
RSR range of 0.10–1.16 has been estimated for world’s forests
and woodlands (IPCC, 2006), while, in a global literature study,
Cairns et al. (1997) reported mean RSRs of 0.24, 0.26 and 0.27 for
tropical, temperate and boreal forest biomes.
The RSR is a practical and cost-effective approach to estimate
CRB. The method is being widely applied, especially in carbon
dynamics studies (e.g. Malhi et al., 2009; Yuen et al., 2013;
Smyth et al., 2013; Doughty et al., 2014), as the significance of
coarse roots to the total belowground biomass and production
becomes more apparent (Clark et al., 2001; Smyth et al., 2013).
RSR has also become particularly useful since there are few avail-
able coarse-root allometric equations that can be extrapolated to
other vegetation types and biomes. The approach is also useful
for the calibration and validation of global and regional dynamic
carbon-cycling models (Mokany et al., 2006). The RSR approach
can however produce biased CRB estimates (Levigne and
Krasowski, 2007; Yuen et al., 2013; Fortier et al., 2015). For
instance, Levigne and Krasowski (2007) recorded greater CRB esti-
mates using allometric equations than from RSRs in A. balsamea
stands in New Brunswick, Canada. They also concluded that there
was more belowground biomass in A. balsamea stands than esti-
mated by the generic RSR often applied to coniferous forests
(Levigne and Krasowski, 2007). This limitation is mainly due to
the high variability that often characterizes RSRs (Mokany et al.,
2006; Poorter and Sack, 2012; Návar, 2015). RSRs may also be
affected by species traits, site, and stand development characteris-
tics (Keith et al., 2000; Barton and Montagu, 2006; Fortier et al.,
2015). According to Keith et al. (2000) most generalized RSRs do
not account for lignotubers, or the influences of resprouting in
some tree species. The use of generalized and mean RSRs may
therefore lead to biased estimates of CRB and carbon dynamics
(e.g. Yuen et al., 2013). There is a general consensus that the use
of site-specific RSRs is more accurate (Mokany et al., 2006;
Levigne and Krasowski, 2007; Sanquetta et al., 2011; Fortier
et al., 2015), and therefore efforts should be made to generate
site-specific ratios for specific forest types in different regions of
the world.
3.1.1.2.3. Ground-Penetrating Radar. One of the emerging indi-
rect techniques to estimate CRB is the use of GPR. GPR is a geo-
physical close-range remote-sensing technique, which uses
electromagnetic waves (EM) to obtain root images (Fisher et al.,
1992; Cui et al., 2011; Butnor et al., 2001, 2012; Guo et al.,
2013a; Samuelson et al., 2015). The principle underlying GPR
operation is the ability of low-frequency radio and microwaves
to penetrate into the subsoil to capture root images (Lorenzo
et al., 2010). A GPR system usually consists of three main compo-
nents – a radar control unit, an antenna and a display unit (Guo
et al., 2013a). During sampling the GPR antenna is moved along
established transects arranged in a grid or any other pattern, and
the EM energy from the antenna propagates into the soil as waves
(Butnor et al., 2012). The transmitted EM signal reflected back from
the roots is digitized, recorded and processed (Lorenzo et al., 2010;
Butnor et al., 2012; Guo et al., 2013a). For an in-depth discussion
on GPR components, operational principles, signal-processing
techniques and GPR-theoretical background see Lorenzo et al.
(2010), Butnor et al. (2001, 2003, 2012) and Guo et al. (2013a).
GPR has been used to estimate CRB in individual trees and stands
in Europe (e.g. Lorenzo et al., 2010), Asia (e.g. Cui et al., 2011;
Hirano et al., 2012) and North America (e.g. Butnor et al., 2001,
2003; Day et al., 2013; Raz-Yaseef et al., 2013; Samuelson et al.,
2015). GPR can also detect and quantify coarse-root spatial
distribution (e.g. Hirano et al., 2012) and tree decay patterns
(Butnor et al., 2009), and determine the physical properties of trees
and soil depth (e.g. Lorenzo et al., 2010). With this approach CRB is
estimated based on an established relationship between GPR
processed radargrams or profiles and destructively sampled root
biomass (Butnor et al., 2003; Day et al., 2013).
GPR has some advantages that make it promising for root stud-
ies. In soils with low organic matter and ion contents, GPR can pro-
duce CRB estimates comparable with other methods. For instance,
Day et al. (2013) reported that GPR-based estimate of CRB was
comparable to soil-pit estimates, and greater than those obtained
from soil cores. The GPR system is portable, and can therefore be
used to scan large areas over a short period of time (Butnor
et al., 2012). GPR can account for large spatial variability of tree
roots within a short time, and can be used to repeatedly monitor
and characterize roots at the same site (e.g. Stover et al., 2007;
Day et al., 2013). This is particularly important since repeated
quantification of root systems in forest and woodland ecosystems
can be very challenging (Bledsoe et al., 1999). GPR can also be uti-
lized with other methods to improve efficiency and accuracy of
root-biomass estimates over large areas (Butnor et al., 2003).
Despite these advantages, successful application of the GPR sys-
tem is usually site-specific (Butnor et al., 2012), and comparisons
between biomass estimates can only be achieved under comparable
root, soil and environmental conditions (Butnor et al., 2001; Guo
et al., 2013b, 2015). GPR-based root-biomass studies have mainly
been conducted in plantations and isolated trees under controlled
conditions (e.g. Cui et al., 2011; Day et al., 2013; Samuelson et al.,
2015). These simplified environments are used because the ability
of the GPR to detect and map roots is directly related to the charac-
teristics of a site (Butnor et al., 2001; Lorenzo et al., 2010). Accord-
ing to Lorenzo et al. (2010), it may be difficult to obtain accurate
GPR data in a dense and highly diverse ecosystem; this precludes
most tropical forest ecosystems that are usually characterized by
diverse structural and life forms. In a Populus deltoides stand in
the Atlantic Coast Flatwoods, Butnor et al. (2001) reported that
GPR was not useful as understory vegetation and other fallen debris
hindered the free movement of the antenna. Samuelson et al.
(2015) circumvented this problem by mowing and raking the
understory of Pinus palustris stands to improve mobility of the
GPR system, but this will not be practicable in many ecosystems.
Successful application of GPR has been limited to well-drained
 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351
sandy soils (e.g. Butnor et al., 2001; Hirano et al., 2012; Day et al.,
2013). According to Guo et al. (2013a), sandy soils with low concen-
trations of organic matter and ions are the most conducive sites for
the use of GPR. The water content of roots is crucial to the detection
of tree roots by GPR (Hirano et al., 2009a; Guo et al., 2013b), as it
closely relates to the dielectric properties of the surrounding soil
(Guo et al., 2013a). Under controlled conditions roots of
Cryptomenia japonica with less than 20% water content were not
identified by GPR (Hirano et al., 2009a). Furthermore GPR may
not be able to distinguish overlapping and closely aligned roots
(Butnor et al., 2001; Hirano et al., 2009a; Guo et al., 2015); these
are often interpreted as a single root, leading to under-estimation
of CRB (Butnor et al., 2001). GPR is also not able to differentiate
roots into size and depth classes; any attempt is confounded by
the roots’ orientation, surface-reflectance geometry, and the close-
ness of untargeted roots (Butnor et al., 2003; Tanikawa et al., 2013;
Guo et al., 2015). It is also difficult to distinguish between live and
dead roots with GPR (Butnor et al., 2001). However, under ideal
conditions, GPR with advanced antenna frequency may detect
(with less precision) decayed roots close to the soil surface (e.g.
Butnor et al., 2005; Zhu et al., 2014). The reliability of GPR estimates
needed to be validated with data from direct root biomass esti-
mates (e.g. Stover et al., 2007; Butnor et al., 2012; Zhu et al.,
2014), and further methodological developments could enhance
the promise of this technique for quantifying root biomass.
3.1.1.2.4. Root biomass increment or difference. This approach
quantifies coarse-root production (CRP) based on changes in CRB
over a specific time period (Sala et al., 1988; Steele et al., 1997),
and production is computed as either the sum of biomass incre-
ments (e.g. Kurz et al., 1996; Kajimoto et al., 1999; Upadhaya
et al., 2005) or the biomass difference (e.g. Haynes and Gower,
1995; Bond-Lamberty et al., 2004; Hermle et al., 2010). Studies
that use biomass increments as an index for production usually
depend on root biomass data from soil cores taken across seasons
for at least one year (e.g. Upadhaya et al., 2005). The latter
approach however quantifies CRP as root biomass difference
obtained from allometric equations (e.g. Bond-Lamberty et al.,
2004; Návar, 2015). Most long-term studies use the biomass differ-
ence index to estimate CRP (e.g. Haynes and Gower, 1995; Hermle
et al., 2010). The use of biomass data to estimate root production is
simple and fast and therefore commonly used in C budget studies
(e.g. Upadhaya et al., 2005; Hermle et al., 2010).
The approach has, however, several limitations; for instance
because it is time-dependent it may under-estimate CRP. The use
of biomass increment for instance mostly ignores contribution of
root mortality and turnover, and losses due to exudation of
C-containing compounds (Kajimoto et al., 1999; Hermle et al.,
2010). This means that values obtained through this approach
are relative, and do not reflect actual roots produced (Sala et al.,
1988). Studies that estimate root production as CRB difference
from allometric equations suffer from the same limitations as the
indirect root-biomass methods. Moreover subtracting two biomass
estimates with their associated error terms can lead to a higher
error for the final value (e.g. Sala et al., 1988; Bond-Lamberty
et al., 2004).
3.1.1.2.5. Fraction or percentage of wood production. One indirect
approach to estimate CRP is as a fraction/percentage of the above-
ground wood production (Law et al., 2001; Malhi et al., 2009;
Girardin et al., 2010; Doughty et al., 2014), based on the assump-
tion of a positive relationship between coarse-root biomass
production and wood production in many ecosystems (Mokany
et al., 2006; Poorter and Sack, 2012). For example, coarse-root pro-
duction was estimated for a mature Pinus ponderosa forest in cen-
tral Oregon by assuming it to be 25% of wood production (Law
et al., 2001). Malhi et al. (2009) multiplied the stem production
estimate by 0.21 to estimate CRP in selected sites in Brazil. This
339
approach is simple, cost-effective and fast, and is increasingly
being applied in carbon cycling and allocation studies, particularly
in the tropics (e.g. Girardin et al., 2010; Doughty et al., 2014). It
may, however, under-estimate CRP since it usually captures only
production of large structural roots (Malhi et al., 2009). The mass
of small coarse roots that are not accounted for by this approach
exceeds that of the large structural roots in many ecosystems
(Clark et al., 2001; Girardin et al., 2010).
3.1.1.2.6. Root radial increment. Recently CRP has been esti-
mated from direct measurements of the radial increment of roots
(e.g. Moser et al., 2010, 2011; Zach et al., 2010). With this in situ
approach, diameter tapes or dendrometer bands are used to record
the diameter increments of superficially growing roots for a given
period (Zach et al., 2010; Moser et al., 2011). For instance, Moser
et al. (2010) manually measured coarse roots with a diameter tape
in a moist montane forest in southern Ecuador, and found that CRB
increased with elevation. When measurements are recorded with
dendrometer bands, the bands are normally mounted on the roots
and monitored for some period before recordings are made. Based
on the diameter data, the relative volume of each root segment is
determined (Moser et al., 2011). These root-volume estimates,
together with root-biomass and stand-density data, are then used
to estimate stand-level CRP (Moser et al., 2010). This approach pro-
vides a direct means to estimate CRP, which may be an important
step toward circumventing the difficulties associated with field
monitoring of coarse roots.
However, this method suffers from the same limitation as allo-
metric equations (Section 3.1.1.2.1), since it fails to capture small
coarse roots (e.g. Moser et al., 2011). In the study of Moser et al.
(2011), only roots with diameters between 20 and 300 mm were
equipped with dendrometer tapes, leading to the conclusion that
CRP was likely under-estimated due to the lack of data from roots
<20 mm in diameter. Another criticism of this method is that dur-
ing sampling, only superficial roots are usually considered (Zach
et al., 2010), but more coarse roots may be distributed in the deep
layers of the mineral soil (e.g. Levillain et al., 2011). Nevertheless,
this method has been employed in the tropics, where visible
aboveground roots and adventitious roots may be common
(Vance and Nadkarni, 1992). Root-production estimates may also
be affected by sampling bias and lack of replication. Despite some
limitations, long-term in situ monitoring of coarse roots with den-
drometer bands holds promise for future carbon dynamics studies
in the tropics.
3.1.2. Fine-root biomass and production
Fine roots (62 mm in diameter) contribute less than coarse
roots to total root biomass (Vogt et al., 1998), but play important
roles in the productivity and biogeochemical cycles of ecosystems.
Fine-root biomass and production have also been estimated by
both direct and indirect methods (Table 2). Direct methods include
soil-core/sequential-coring, monolith, soil-pit, ingrowth-core and
(mini) rhizotrons, while indirect approaches include N-budget,
pipe-model and other empirical models.
3.1.2.1. Direct methods.
3.1.2.1.1. Soil-core. Fine-root biomass (FRB) is commonly esti-
mated by the soil-core method (Bledsoe et al., 1999; Makkonen
and Helmisaari, 1999; Oliveira et al., 2000). Soil cores or augers
are usually used to sample fine roots, depending on the availability
of equipment and investigator preference. One of the most impor-
tant considerations is the diameter of the corer or auger used for
sampling roots (Oliveira et al., 2000; Snowdon et al., 2002). Accord-
ing to Oliveira et al. (2000) the diameter of a corer should provide a
good balance between sampling accuracy and intensity. Commonly
used core diameters range from 1.9 to 15 cm (Oliveira et al., 2000;
Levillain et al., 2011), but Snowdon et al. (2002) recommended
340 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351
corers of diameter >10 cm to estimate FRB. Field sampling may be
based on random, systematic or stratified-random designs; an
important consideration in designing field-sampling procedures
is to avoid clumping of sampling locations so as to capture the spa-
tial heterogeneity of root distribution in ecosystems. The depth to
which root cores are taken is crucial for accurate and reliable
determination of FRB. Ideally, fine roots should be sampled to the
maximum root-depth limit for the site (Bledsoe et al., 1999;
Oliveira et al., 2000), but this may not always be possible, particu-
larly at sites with stony soils (Park et al., 2007). Sampling depth
should therefore be informed by a preliminary assessment of the
concentration of fine roots at each depth.
The soil-core method has been extensively used to estimate FRB
for decades (see Vogt et al., 1998; Yuan and Chen, 2012a), and is
preferred by most investigators (e.g. Bledsoe et al., 1999; Park
et al., 2007). The utility of the soil-core method is its simplicity
and its ability to capture well the spatial and temporal heterogene-
ity in FRB distribution over large scales (e.g. Makkonen and
Helmisaari, 1999). According to Makkonen and Helmisaari
(2001), soil cores are preferred for the study of annual and seasonal
variations in FRB. Root-biomass data from the soil-core method is
also used to validate the efficiency and accuracy of other methods
(e.g. Day et al., 2013).
The soil-core method has limitations that affect its field applica-
tion and the estimates of FRB, and may over- or under-estimate
FRB estimates. Soil compaction, which is a common problem with
the use of cores, can result in over-estimation of root biomass. For
example, compaction resulted in 10% over-estimation of FRB in a
naturally regenerated hardwood forest in New Hampshire (Park
et al., 2007). However, using a core with a large inner diameter
may reduce soil compaction and improve root-biomass estimates
(Bledsoe et al., 1999), but the use of large diameter cores in rocky
or stony sites may be difficult (Park et al., 2007).
The difficulty in separating organic debris from fine roots may
lead to over-estimation of root biomass (Millikin and Bledsoe,
1999; Snowdon et al., 2002). Extracting sample cores and root-
processing (washing, sorting, weighing) takes considerable time,
so in most studies roots are under-sampled, which affects the reli-
ability of FRB data (Metcalfe et al., 2007b; Levillain et al., 2011;
Berhongaray et al., 2013; Taylor et al., 2013). In a study of a Euca-
lyptus plantation in Congo, Levillain et al. (2011) sampled 312
auger cores from the soil surface (0–10 cm) to achieve a 10% preci-
sion. In a young short-rotation Populus plantation in Belgium,
Berhongaray et al. (2013) found that when processing extracted
cores that the time spent washing, sorting and weighing roots rep-
resented 84–93% of the total time needed to process root samples.
The high number of core samples required to get a good precision,
as well as the processing time makes soil cores expensive and
impractical in highly replicated experiments (Bledsoe et al.,
1999). Field sampling and laboratory techniques such as random-
ization, temporal prediction and diameter-class accumulation
curves have been developed to improve field and laboratory effi-
ciency and, to reduce root-processing time (e.g. Metcalfe et al.,
2007b; Berhongaray et al., 2013; Taylor et al., 2013).
3.1.2.1.2. Monolith. Fine-root biomass has also been quantified
with the monolith sampling method (e.g. Lawson et al., 1970;
Kimmins and Hawkes, 1978; Oliveira et al., 2000; Levillain et al.,
2011; Gautam and Mandal, 2012). The method requires cutting
of a monolith (block) of the soil directly from the soil surface, or
at different depths, from the wall of a trench. Soil monoliths can
also be excavated with frames constructed from wooden or metal-
lic materials (Oliveira et al., 2000; Ibrahima et al., 2010). Investiga-
tors should conduct preliminary assessments to ensure that the
size and number of monoliths is sufficient to account for the
heterogeneity of root distribution at the site before using them in
a large study.
Monoliths have some advantages – they provide large soil sam-
ple volumes, which increase the accuracy of FRB estimates (Taylor
et al., 2013), and reduce the number of replicates needed to secure
good estimates of FRB (Levillain et al., 2011). In a Eucalyptus plan-
tation in Congo, 127 monoliths of volume 25 cm " 25 cm " 10 cm
were required to achieve 10% sampling precision (Levillain et al.,
2011). For 30% precision, the number of soil blocks required fell
to 14, which could be accomplished in one person-day (Levillain
et al., 2011). Monoliths are also suited for sites where roots may
be distributed into the deep layers of the soil (Levillain et al., 2011).
The monolith method is, however, beset with limitations
(Table 2). Apart from being time-consuming and laborious, it can
produce erroneous estimates of FRB due to inappropriate washing
and oven-drying procedures. Because monoliths collect large soil
volumes, it may be practically difficult to completely remove min-
eral particles attached to lower-order roots. Larger losses may also
occur during washing, particularly in cases where frames are used
to sample roots (Oliveira et al., 2000). There is, therefore, the need
to apply a correction factor to account for root loss and adhering
mineral particles, in order to obtain a comparable biomass esti-
mate (e.g. Kimmins and Hawkes, 1978). The monolith method also
requires considerable time for sorting and processing of fine roots.
Levillain et al. (2011) reported that sieving operations related to
monolith root extraction took 31 person-days, accounting for
about 55% of the time spent on field sampling and processing.
Under unfavourable conditions, soil blocks may collapse during
excavation, which will increase the time spent in the field (e.g.
Makita et al., 2011). Finally, excavation of soil blocks from deep soil
layers along a trench was impossible in a broad-leaved deciduous
forest in Japan because the soil was hardened (Makita et al., 2011).
3.1.2.1.3. Ingrowth-core. The root-ingrowth core (Persson,
1979), including various modifications (e.g. Vogt et al., 1998;
Hirano et al., 2009b; Lukac and Godbold, 2010; Li et al., 2013;
Milchunas, 2012; Wang et al., 2014; Van Do et al., 2015) is one
of the most commonly used methods to estimate fine-root produc-
tion and turnover. The method estimates the amount of fine root
that grows into a defined volume of root-free soil within a specified
period of time. Its field application is based on the assumption that
disturbances of roots and the surrounding soil during core, or net
installation, do not affect root production during the ingrowth per-
iod (Lauenroth, 2000). This assumption may not apply in all sites
and forest types (e.g. Hendricks et al., 2006). Studies have generally
found that the method provides conservative root-biomass esti-
mates, and could under-estimate FRP compared to sequential-
coring and (mini) rhizotrons (see Appendix B). This may be due
to constraints of mesh size on root ingrowth and rapid turnover
of roots, which is missed before sampling (Hertel and Leuschner,
2002; Adamek et al., 2011; Milchunas, 2012). The ingrowth-core
method may, however, provide fine-root production estimates
comparable to other methods if the time elapsed between cores
installation and root sampling is long enough to allow for maxi-
mum root colonization (e.g. Makkonen and Helmisaari, 1999;
Ostonen et al., 2005; Jourdan et al., 2008). This is a very important
consideration, particularly for sites with strong seasonal fluctua-
tions in root growth. Despite these potential limitations, the
ingrowth-core is used extensively because it is inexpensive and
field-application is simple and straightforward. It is considered to
be most effective in ecosystems with fast root growth such as
the tropics (Vogt et al., 1998).
3.1.2.1.4. (Mini) rhizotrons. Rhizotrons or minirhizotrons allow
for fast and continuous in situ measurement of roots and root seg-
ments with moderate disturbance to sites (Taylor et al., 1990;
Hendrick and Pregitzer, 1996; Vogt et al., 1998; Bernier and
Robitaille, 2004). The two techniques are considered together
because they both employ transparent interfaces, and the field
applications involve similar processes, which include installation,
 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351
root image collection, data processing, and conversion of root-
growth parameters into biomass production (Taylor et al., 1990;
Madji, 1996; Milchunas, 2012; Girardin et al., 2013).
Minirhizotron involves inserting clear tubes (usually small in
size) into the ground at an angle, and a device such as camera is
used to observe and capture root-growth at the soil-tube interface
(Vogt et al., 1998; Roberti et al., 2014). Rhizotrons also have clear
windows or screens installed on or both sides of soil profiles dug
to a certain depth (Taylor et al., 1990; Fahey and Hughes, 1994;
Metcalfe et al., 2007a), and fitted with materials such as black plas-
tic sheets to mimic natural soil conditions. Root-growth is captured
on the outer surface of the window or screen by either scanning or
taking photos or manually tracing visible roots onto transparent
sheets (Vogt et al., 1998; Janos et al., 2008; Girardin et al., 2013).
Novel approaches that incorporate geographical information sys-
tems and remote-sensing techniques have been proposed to
improve data capture and processing time (e.g. Silva, 2014). The
root images or drawings are usually analyzed with software pro-
grams (Hendricks et al., 2006; Lobet et al., 2013). Lobet et al.
(2013) identified 19 software programs that can be used to analyze
root systems of plants. Since (mini) rhizotrons cannot directly pro-
duce FRB estimates, different approaches have been developed to
convert root-growth data into mass production (Vogt et al.,
1998; Bernier and Robitaille, 2004; Hendricks et al., 2006;
Metcalfe et al., 2007a). The conversion used may, however, influ-
ence the accuracy of FRP estimates (Metcalfe et al., 2007a). Several
studies have reported significantly greater FRP estimates from
(mini) rhizotrons compared to other methods (e.g. Fahey and
Hughes, 1994; Steele et al., 1997; Finér et al., 2011; Girardin
et al., 2013). However, Moser et al. (2010) recorded higher FRP esti-
mates for ingrowth-core compared to minirhizotron in Ecuadorian
tropical montane forests.
The main disadvantage of rhizotron methods is the substantial
cost involved in acquiring equipment and processing the root data.
Hendrick and Pregitzer (1996) estimated the combined cost of
minirhizotron and data-processing equipment to be more than
$US 15,000. Current costs would be substantially higher, which
would be a major hindrance to many investigators. Installation of
the minirhizotron tubes or rhizotron screens may change water
regimes and soil matrix resistance to root penetration, which
would affect the production estimates (Taylor et al., 1990;
Hendricks et al., 2006). Root production can also be under-
estimated due to inappropriate scaling and calculation of soil vol-
ume sampled by minirhizotron images (Taylor et al., 2014). Root
growth and mortality may also be stimulated along the tubes or
screens of (mini) rhizotrons (Hendrick and Pregitzer, 1996;
Milchunas, 2012). Moreover a large number of (mini) rhizotron
tubes or screens may be required to properly capture root biomass
distribution in highly heterogeneous sites.
3.1.2.1.5. Sequential-coring. Fine-root production can also be
estimated by sampling soil cores at specific-time intervals for at
least one year, and calculating the difference in biomass and necro-
mass between the two periods (Vogt et al., 1998; Lauenroth, 2000;
Olesinski et al., 2012). Each approach requires collecting root bio-
mass, necromass or decomposition data independently or in com-
bination before it can be applied to calculate FRP (Vogt et al., 1998).
Among the three approaches the most widely used is the Mini-
mum–Maximum formula, and the least is the Compartment Flow
(Jourdan et al., 2008; Hertel and Leuschner, 2002; Hendricks
et al., 2006; Finér et al., 2011; Yuan and Chen, 2012a; Brunner
et al., 2013), which requires additional root-decomposition data
to calculate FRP (Vogt et al., 1998). However the Compartment
Flow formula may produce higher FRP estimates relative to the
others (e.g. Hertel and Leuschner, 2002; Berhongaray et al.,
2013). There are suggestions that the Minimum–Maximum for-
mula may not be suitable for tropical ecosystems because of low
341
seasonality in fine-root growth (Moser et al., 2010). New
approaches such as forward, backward and continuous inflow esti-
mates have also been developed to calculate FRP from sequential-
coring data (e.g. Osawa and Aizawa, 2012; Van Do et al., 2015). The
sequential-coring method can also be used to estimate mycorrhizal
biomass and production (Vogt et al., 1998). The main disadvantage
of sequential coring is that it may over- or under-estimate FRP
(Hertel and Leuschner, 2002; Milchunas, 2012), because it assumes
that fine-root biomass production and mortality occur asyn-
chronously (Vogt et al., 1998; Lauenroth, 2000), although in many
ecosystems the opposite trend is observed (e.g. Hendricks et al.,
2006). Sequential-coring is also expensive and laborious, requiring
a large number of soil-core replicates to produce good estimates.
3.1.2.2. Indirect methods.
3.1.2.2.1. The pipe model and others. FRB of individual trees and
stand can be estimated indirectly with models including the pipe
model (Shinozaki et al., 1964a; Niiyama et al., 2010). This is based
on the pipe-model theory of tree form, which views a tree as an
assemblage of pipe systems from the bottom to the top of the tree
(Shinozaki et al., 1964a, 1964b). The contiguous nature of the pipes
in a tree ensures that the cross-sectional area of an organ remains
constant, even during branching events. The assumption of self-
preservation in roots allows for the development of a simple model
to predict root biomass (e.g. Carlson and Harrington, 1987;
Richardson and Zu Dohna, 2003; Niiyama et al., 2010). For in-
depth discussion on the assumptions, theoretical justifications
and calculations of the pipe model refer to Shinozaki et al.
(1964a, 1964b) and Niiyama et al. (2010). The pipe model has
rarely been used to determine FRB (e.g. Carlson and Harrington,
1987; Niiyama et al., 2010), although it is has been presented as
a fast, non-destructive alternative approach to estimate FRB
(Carlson and Harrington, 1987).
FRB can also be estimated from other models based on easily
measurable aboveground metrics such as basal diameter, DBH,
height and crown foliage. These models function on the basis of a
strong relationship between FRB and aboveground variables at
both tree and stand-levels (e.g. Kurz et al., 1996; Chen et al.,
2004; Lee et al., 2004; Sun et al., 2015), although this may not
apply to all sites (e.g. Helmisaari et al., 2007). Several models have
been developed and used to predict FRB (e.g. Ammer and Wagner,
2002, 2005; Zerihun et al., 2007; Jurasinski et al., 2012). Models are
a cost-effective means of determining FRB, particularly at large
spatial scales (e.g. Kurz et al., 1996), at which aboveground biomet-
ric data may be the only available and dependable data available
for most ecosystems. Chen et al. (2004) reported a good correlation
between measured and model-estimated FRB of selected tree spe-
cies from boreal and temperate forests. Unlike destructive meth-
ods, the accuracy of models does not depend on the spatial
variation in root distribution in a stand (Lee et al., 2004).
The use of models to predict FRB has some limitations, leading
to uncertainties in the estimates they produce (e.g. Zerihun et al.,
2007; Jurasinski et al., 2012). Models are unable to reflect the high
temporal and spatial heterogeneity in FRB distribution common in
most ecosystems (e.g. Ammer and Wagner, 2005; Helmisaari et al.,
2007; Zerihun et al., 2007). Finally, some of the assumptions used
to parameterize models may not hold true for all tree species and
ecosystems (e.g. Ammer and Wagner, 2002; Lee et al., 2004).
3.1.2.2.2. N budget. The N-budget approach measures FRP as the
product of annual N allocation to fine roots and the C:N ratio in fine
roots (Nadelhoffer and Raich, 1992; Hendricks et al., 2006). This is
based on the assumption that FRP can be predicted from N alloca-
tion since root production is largely driven by soil N (Nadelhoffer
and Raich, 1992). To use this approach, complete data on N input,
pools and fluxes at the ecosystem level must be available (Vogt
et al., 1998; Hendricks et al., 2006). Several assumptions have to
342 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351

2.5 5
(a)
Coarse-root biomass (Mg/ha)

Fine-root production (Mg/ha/yr)

2.0 4

1.5
3

1.0
2
0.5

1
0.0
Soil-pit Soil-core
Method 0
Ingrowth-core (Mini) rhizotrons Sequential-coring
Method
1.5
(b)
log 10 y = 0.63 x log 10 x + 0.19 Fig. 3. Fine-root production estimates (Mg ha!1 year!1) (mean ± S.E) from
ingrowth-core (n = 73), (mini) rhizotrons (n = 26) and sequential-coring (n = 59)
r 2 = 0.32
methods. Data represent all observations used in the study.
p = 0.07
1.0
Soil-core

methods were not significantly different (t = 0.06, p = 0.96, n = 11)

0.5
0.0
0.0
Fig. 1. (a) Coarse-root (>2 mm) biomass estimates (Mg ha!1) (mean ± S.E) from
soil-pit and soil-core methods, and (b). Relationship between coarse-root biomass
estimates from (Mg ha!1) (mean ± S.E) from soil-pit and soil-core methods (n = 11).
Broken line is 1:1 relationship between the methods. Data were derived from the
same sites, and correlation values are log-transformed (base 10).
be satisfied to use the approach, including N limitation of plant
growth (Vogt et al., 1998), which is not the case in many ecosys-
tems (e.g. Cleveland et al., 2011). This technique has rarely been
used to estimate FRP (see Finér et al., 2011; Yuan and Chen,
2012a), and there are suggestions that its application should be
limited to ecosystems with conditions similar to the N-poor sites
for which it was developed (Vogt et al., 1998).
3.2. Comparison of methods
3.2.1. Coarse-root biomass estimates from soil-pit and soil-core
methods
In the dataset of eleven sites evaluated during this study
(Appendix A) estimates of mean CRB from soil-pit and soil-core
(Fig. 1a), and were positively correlated (r2 = 0.32, p = 0.07,
n = 11) (Fig. 1b). However, in a study of a 6-year-old Eucalyptus
plantation, Levillain et al. (2011) found slightly higher CRB
estimates using soil-pits compared to soil-cores and concluded
that auger coring was not a suitable method for estimating CRB.
In contrast, Smith et al. (2013) reported a significant positive
0.5 1.0 1.5
correlation (r2 = 0.40, p < 0.001) between CRB estimates from
Soil-pit 30 " 30 " 30 cm soil pits and 8-cm-diameter soil cores in a
CO2-enrichment study in the UK. The different results observed
in these aforementioned studies could be explained by differences
in the tree planting densities. Smith et al. (2013) used a planting
density of 15,000 stems ha!1 to expedite tree ecological interac-
tions whereas a density of 800 stems ha!1 was used by Levillain
et al. (2011). The high planting density could have reduced the
spatial heterogeneity of coarse roots.
Spatial heterogeneity of coarse root distribution and sampling
strategies are major confounding factors when estimating in situ
CRB. Estimates produced by the aforementioned techniques (see
Section 3.1.1) can vary widely and can be altered by planting den-
sity, site conditions, tree allometry, tree developmental age, site
specific environmental conditions, or species specific differences
(Resh et al., 2003). Indeed, the most detailed spatial sampling
designs rarely captures the fact that the majority of coarse roots
are concentrated below the tree stem potentially resulting in a sig-
nificant under-estimate of CRB. As suggested by Resh et al. (2003)
we support the assertion that, where destructive harvesting
permits, the lowest cost method to achieve a high accuracy CRB

10
8
(a) (b)
Fine-root biomass (Mg/ha)

8
6
6
Soil-core

4
4 y = 0.82x + 1.65

2
r 2 = 0.91
2 p < 0.0001

0 0
Soil-pit Soil-core 0 2 4 6 8 10
Method Soil-pit

Fig. 2. (a) Fine-root (62 mm) biomass estimates (Mg ha!1) (n = 9) from soil-pit and soil-core methods, and (b). Relationship between fine-root biomass estimates from soil-
pit and soil-core (Mg ha!1) (n = 11). Broken line is 1:1 relationship between the methods. Data were derived from the same sites.
 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351 343

estimation is a combination of soil coring and root ball
excavation. Interpretation of coarse root data must include a
consideration of the sampling technique used to ensure
that under-estimates of CRB are not biased by techniques that do
not account for the high concentration of coarse roots below the
tree bole.
3.2.2. Fine-root biomass estimates from soil-pit and soil-core methods
The mean FRB estimate from the dataset in Appendix A was
higher for soil cores (5.17 ± 0.93 Mg ha!1) than the estimate from
soil pits (4.31 ± 0.08 Mg ha!1), but the difference was not signifi-
cant (t = 0.601, p = 0.556, n = 9) (Fig. 2a). Many studies at single
2.5
log10 y = 0.48 x log10x + 0.37
2.0 r 2 = 0.26
p < 0.0001
Ingrowth-core
sites have reported higher FRB estimates from the soil-core com-
pared to the soil-pit method (e.g. Millikin and Bledsoe, 1999;
Park et al., 2007 and references herein). There was a significant
positive correlation between FRB estimates obtained from soil-
core and soil-pit methods (Fig. 2b), which may indicate the utility
of both methods to quantify FRB. Some investigators (e.g. Bledsoe
et al., 1999; Park et al., 2007) recommend the use of soil-core
method to quantify FRB, due to its simplicity and other advantages,
discussed in Section 3.1.2.1.1.
3.2.3. Fine-root production estimates from ingrowth-core, (mini)
rhizotrons and sequential-coring methods
The mean FRP estimate obtained from studies in Appendix B
was lower in the ingrowth-core method (2.06 ± 0.23 Mg ha!1
year!1, n = 73) compared to estimates provided by (mini) rhi-
zotrons (3.81 ± 0.46 Mg ha!1 year!1, n = 26) and sequential-coring
methods (3.84 ± 0.93 Mg ha!1 year!1, n = 59) (Fig. 3), although
the differences were not significant (F = 2.851, p = 0.061). Earlier
reviews and single studies that compared the three methods have

1.5
also reported lower FRP estimates from ingrowth-core than from
other methods (e.g. Vogt et al., 1998; Hendricks et al., 2006;
1.0 Moser et al., 2010; Finér et al., 2011). Likewise, Finér et al. (2011)
reported higher FRP estimates for sequential-coring and (mini) rhi-
0.5 zotrons methods than the ingrowth-core method, although there
were no significant differences in FRP estimates among the three
(a)
methods at the stand level (Finér et al., 2011).
0.0
There was a significant positive correlation between FRP esti-
0.0 0.5 1.0 1.5 2.0 2.5
mates obtained from sequential-coring and ingrowth-core
Sequential-coring (Fig. 4a), and ingrowth-core and (mini) rhizotrons (Fig. 4b), as well
a sequential-coring and (mini) rhizotrons methods (Fig. 4c). For
2.0 instance, Yuan and Chen (2012b) reported similar patterns of FRP
between sequential-coring and ingrowth-core methods in a boreal
mixed forest in Ontario, Canada, but others have reported contrast-
1.5 ing relationships between sequential-coring and other methods
(Mini) rhizotrons

(e.g. Steele et al., 1997; Hendricks et al., 2006; Moser et al.,

2010). The methods explained less than 50% of the variation in
1.0 FRP, indicating influences of other factors such as species, site
conditions, sampling depth, fine-root size classification, resource
log10 y =0.42 x log10 x + 0.83 availability, stand and environmental conditions on FRP (Rytter,
0.5 r2 = 0.44
1999; Makkonen and Helmisaari, 2001; Ostonen et al., 2005;
p = 0.0003
Hendricks et al., 2006; Finér et al., 2011; Mei et al., 2010; Yuan
(b) and Chen, 2010, 2012b; Smith et al., 2013).
0.0
0.0 0.5 1.0 1.5 2.0
Ingrowth-core 4. Conclusions

2.5 There is currently no consensus as to how to best estimate root

biomass and production. Many investigators prefer root-
excavation and soil-pit methods to estimate CRB, despite the high
2.0
cost and labor required. GPR is a promising indirect approach to
(Mini) rhizotrons

quantify CRB, but may not suitable for ecosystems with a dense
1.5 understory and soils with high organic matter and ion contents.
Empirical models are widely used to predict fine- and coarse-
1.0 root biomass and production in carbon studies. Comparative stud-
log10 y = 0.21 x log 10x + 1.05 ies have shown a consistent relationship between FRB estimates
r 2 = 0.37 from the soil-pit and soil-core methods. For FRP, the ingrowth-
0.5
p = 0.05 core method consistently provided lower estimates than other
(c) methods. Based on the reviewed literature and comparative analy-
0.0 sis we propose the following: (i) the soil-pit method should be
0.0 0.5 1.0 1.5 2.0 2.5 employed to estimate coarse-root biomass because it can serve
Sequential-coring as a compromise between cost and efficiency; (ii) (mini) rhizotrons
should be favored over the other methods to estimate fine-root
Fig. 4. Relationship between fine-root production estimates (Mg ha!1 year!1) from production; (iii) where cost and site conditions (e.g. in stony or
(a) sequential-coring and ingrowth-core (n = 58), (b) ingrowth-core and (mini)
rhizotrons (n = 25), and (c) sequential-coring and (mini) rhizotrons (n = 11)
on steep slopes) preclude the use of (mini) rhizotrons, the
compared at the same sites. Values of fine-root production are log- transformed sequential-coring and ingrowth-core methods are suitable; (iv)
(base 10). Broken line is 1:1 relationship between the methods. the ingrowth-core method should be used with caution in sites
344 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351

where root growth is influenced by strong seasonal fluctuations, Acknowledgements

and when used, the period between cores/nets installation and
root sampling should be extended to allow for maximum root col-
onization; and (v) multiple methods should be employed to esti-
mate fine-root production, and more comparative studies of
different methods on the same sites are needed.
This work was supported by a University of British Columbia
Doctoral Fellowship, the Natural Resources Environment Research
Council (NERC) of UK, the Government of Ghana through the Coun-
cil for Scientific and Industrial Research, and the International
Foundation for Science, Stockholm, Sweden, through a grant to
Shalom D. Addo-Danso.

Appendix A. Data used in the analysis of fine-and coarse-root biomass, including references

Site/location Biome Stand Root biomass Sampling Root Reference

age (Mg ha!1) depth (cm) size
(year) (mm)
Fine-root biomass
Prunus pensylvanica–Betula papyrifera–Fagus Temperate 14 4.20a 10 <2 Park et al.
grandifolia young stand 1, New Hampshire, USA 4.80b 10 (2007)
Fagus grandifolia–Acer rubrum mixed young stand 2, Temperate 16 4.17a 10 <2 Park et al.
New Hampshire, USA 6.40b 10 (2007)
Betula papyrifera–Populus tremuloides–Acer rubrum Temperate 26 5.25a 10 <2 Park et al.
mixed old stand 1, New Hampshire, USA 6.40b 10 (2007)
Betula alleghaniensis–Fagus grandifolia–Acer rubrum Temperate 29 4.48a 10 <2 Park et al.
mixed old stand, New Hampshire, USA 5.20b 10 (2007)
Quercus douglasii woodland, California, USA Temperate – 0.30a 100 <2 Millikin and
2.30b 50 Bledsoe (1999)
Eucalyptus urophylla and Eucalyptus grandis clonal Tropical 6 1.30a 300 <2 Levillain et al.
plantation, Pointe-Noire, Congo 1.20b 100 (2011)
Artemisia tridentate vesayama–Pinus monophylla Temperate – 8.80a 52 <2 Rau et al.
woodland, Nevada, USA 9.30b (2009)
Montane wet forest, Monteverde, Costa Rica Tropical – 9.40a 85–180 <2 Vance and
8.40b 20 Nadkarni
(1992)
Pinus radiate plantations, Canberra, Australia Temperate 10–34 0.87a 30 <3 Moir and
2.50b Bachelard
(1969)
Coarse-root biomass
Eucalyptus urophylla and Eucalyptus grandis clonal Tropical 6 1.93a 300 2–10 Levillain et al.
plantation, Pointe-Noire, Congo 1.34b 100 (2011)
Artemisia tridentate vesayama–Pinus monophylla Temperate – 0.30a 52 >2 Rau et al.
woodland, Nevada, USA 2.30b (2009)
Quercus douglasii woodland, California, USA Temperate – 2.70a 52 >2 Millikin and
0.60b Bledsoe (1999)
Alnus glutinosa monoculture stand, ambient CO2, Temperate 0.87a 30 >2 Smith et al.
Bangor, Wales 0.66b (2013)
Betula pendula monoculture stand, ambient CO2, Temperate 3 0.86a 30 >2 Smith et al.
Bangor, Wales 2.85b (2013)
Fagus sylvatica monoculture stand, ambient CO2, Temperate 3 0.89a 30 >2 Smith et al.
Bangor, Wales 0.88b (2013)
Alnus glutinosa–Betula pendula–Fagus sylvatica, Temperate 3 1.56a 30 >2 Smith et al.
mixed stand, ambient CO2, Bangor, Wales 1.23b (2013)
Alnus glutinosa monoculture stand, elevated CO2, Temperate 3 0.79a 30 >2 Smith et al.
Bangor, Wales 1.00b (2013)
Betula pendula monoculture stand, elevated CO2, Temperate 3 1.59a 30 >2 Smith et al.
Bangor, Wales 1.08b (2013)
Fagus sylvatica monoculture stand, elevated CO2, Temperate 3 0.32a 30 >2 Smith et al.
Bangor, Wales 0.35b (2013)
Alnus glutinosa–Betula pendula–Fagus sylvatica, Temperate 3 2.90a 30 >2 Smith et al.
mixed stand, elevated CO2, Bangor, Wales 4.48b (2013)
Methods: a = soil-pit; b = soil-core.
 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351 345

Appendix B. Data used in the analysis of fine-root production, including references

Site/location Biome Stand Fine-root Sampling Fine-root Study Reference

age production depth size duration
(year) (Mg ha!1 yr!1) (cm) (mm) (year)
Montane forest, 1000 m. a.s.l. Tropical – 4.84a 30 <2 1 Girardin et al. (2013)
Eastern Andes, Peru 4.84b
Montane forest, 1500 m. a.s.l. Tropical – 3.40a 30 <2 1 Girardin et al. (2013)
Eastern Andes, Peru 7.24b
Montane forest, 1855 m. a.s.l. Tropical – 6.52a 30 <2 1 Girardin et al. (2013)
Eastern Andes, Peru 5.98b
Montane forest, 2020 m. a.s.l. Tropical – 3.60a 30 <2 1 Girardin et al. (2013)
Eastern Andes, Peru 4.84b
Montane forest, 2720 m. a.s.l. Tropical – 3.24a 30 <2 1 Girardin et al. (2013)
Eastern Andes, Peru 4.34b
Montane forest, 3020 m. a.s.l. Tropical – 2.62a 30 <2 1 Girardin et al. (2013)
Eastern Andes, Peru 5.60b
Montane forest, 3025 m. a.s.l. Tropical – 4.16a 30 <2 1 Girardin et al. (2013)
Eastern Andes, Peru 8.50b
Montane forest, 1050 m. a.s.l. Tropical – 3.62a 30 <2 1 Moser et al. (2010)
Southern Andes, Ecuador 2.28b
2.05c
Montane forest, 1540 m. a.s.l. Tropical – 9.06a 30 <2 1 Moser et al. (2010)
Southern Andes, Ecuador 3.16b
4.91c
Montane forest, 1890 m. a.s.l. Tropical – 7.02a 30 <2 1 Moser et al. (2010)
Southern Andes, Ecuador 2.97b
14.48c
Montane forest, 2380 m. a.s.l. Tropical – 6.10a 30 <2 1 Moser et al. (2010)
Southern Andes, Ecuador 3.72b
23.91c
Montane forest, 3060 m. a.s.l. Tropical – 3.78a 30 <2 1 Moser et al. (2010)
Southern Andes, Ecuador 9.40b
48.77c
Lowland terra firme forest, Tropical – 3.70a 30 <2 1 Metcalfe et al. (2007a,
Caxiauanã, Brazil 6.03b 2007b)
Mixed hardwood forest, New Temperate >100 5.10a 30 61 1 Fahey and Hughes
Hampshire, USA 2.10b (1994)
Picea mariana plantation, Manitoba, Boreal 150– 0.53a 30 <2 1 Steele et al. (1997)
Canada 155 1.74b
Pinus banksiana plantation, Boreal 65–70 0.29a 30 <2 1 Steele et al. (1997)
Manitoba, Canada 1.90b
Populus tremuloides plantation, Boreal 50–55 0.45a 30 <2 1 Steele et al. (1997)
Manitoba, Canada 0.88b
Picea mariana plantation, Boreal 110– 0.66a 30 <2 1 Steele et al. (1997)
Saskatchewan, Canada 120 2.35b
Pinus banksiana plantation, Boreal 65–70 0.24a 30 <2 1 Steele et al. (1997)
Saskatchewan, Canada 2.09b
Populus tremuloides plantation, Boreal 65–70 0.73a 30 <2 1 Steele et al. (1997)
Saskatchewan, Canada 0.58b
Pinus palustris–Aristida beyrichiana Temperate – 0.80a 35 60.5 1 Hendricks et al. (2006)
forests, Hydric site, Georgia, USA 4.62b 51
0.78c 30
Pinus palustris–Aristida beyrichiana Temperate – 1.06a 35 60.5 1 Hendricks et al. (2006)
forests, Mesic site, Georgia, USA 1.91b 51
0.83c 30
Pinus palustris–Aristida beyrichiana Temperate – 1.48a 35 60.5 1 Hendricks et al. (2006)
forests, Xeric site, Georgia, USA 2.30b 51
0.81c 30
Cryptomeria japonica coniferous Temperate >15 3.20b – <1 – Noguchi et al. (2007)
plantations, Japan 0.72c
Chamaecyparis obtuse plantations, Temperate >15 2.43a – <1 – Noguchi et al. (2007)
Japan 0.18c

(continued on next page)

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Appendix B (continued)
Site/location Biome Stand Fine-root Sampling Fine-root Study Reference
age production depth size duration
(year) (Mg ha!1 yr!1) (cm) (mm) (year)
Deciduous plantations, Japan Temperate >15 3.85a – <2 – Noguchi et al. (2007)
3.78b <1
Salix viminalis short-rotation Boreal 5 5.20b 50 62 1 Rytter (1999)
plantation, Ultuna, Sweden 1.60c
Picea abies plantation, Roela, Estonia Boreal 60 0.97a 40 62 3 Ostonen et al. (2005)
2.51c 30
Pinus sylvestris stands, Central Boreal 120 2.26a – 62 – Persson (1983)
Sweden 2.17c
Quercus laurifolia–Quercus alba– Temperate 78 3.54a 40 <2 1 Powell and Day (1991)
Liquidambar styraciflua swamp 9.89c
forests, North Carolina, USA
Chamaecyparis thyoides swamp Temperate 57 2.74a 40 <2 1 Powell and Day (1991)
forest, North Carolina, USA 3.66c
Nyssa aquatica–Acer rubrum swamp Temperate 52 0.91a 40 <2 1 Powell and Day (1991)
forest, North Carolina, USA 0.59c
Pinus koraiensis mixed forests Temperate 200 0.56a 20 <2 1 Wang et al. (2012)
(unfertilized stand), Changbai 4.99c
mountain, China
Pinus koraiensis mixed forests Temperate 200 0.17a 20 <2 1 Wang et al. (2012)
(fertilized stand), Changbai 5.73c
mountain, China
Larix gmelinii plantation Temperate 16 0.20a 30 61 1 Mei et al. (2010)
(unfertilized), Heilongjiang, China 1.25c
Larix gmelinii plantation (fertilized), Temperate 16 0.06a 30 61 1 Mei et al. (2010)
Heilongjiang, China 1.13c
Fraxinus mandshurica plantation Temperate 16 1.55a 30 61 1 Mei et al. (2010)
(unfertilized), Heilongjiang, China 1.76c
Fraxinus mandshurica plantation Temperate 16 0.71a 30 61 1 Mei et al. (2010)
(fertilized), Heilongjiang, China 1.86c
Populus tremuloides–Picea mariana Boreal 3 0.90a 30 62 1 Yuan and Chen
mixed forests, Ontario, Canada 1.50c (2012b)
Populus tremuloides–Picea mariana Boreal 11 1.60a 30 62 1 Yuan and Chen
mixed forests, Ontario, Canada 3.10c (2012b)
Populus tremuloides–Picea mariana Boreal 29 1.10a 30 62 1 Yuan and Chen
mixed forests, Ontario, Canada 2.10c (2012b)
Populus tremuloides–Picea mariana Boreal 94 0.50a 30 62 1 Yuan and Chen
mixed forests, Ontario, Canada 1.60c (2012b)
Populus tremuloides–Picea mariana Boreal 142 0.60a 30 62 1 Yuan and Chen
mixed forests, Ontario, Canada 1.30c (2012b)
Populus tremuloides–Picea mariana Boreal 205 0.70a 30 62 1 Yuan and Chen
mixed forests, Ontario, Canada 1.40c (2012b)
Lowland terra firme, clay loam site, Tropical – 3.02a 20 <2 2.2 Jiménez et al. (2009)
Caatinga, Columbia 2.72c
Lowland terra firme, sandy loam Tropical – 5.97a 20 <2 2.2 Jiménez et al. (2009)
site, Caatinga, Columbia 6.67c
Populus tremuloides–Pinus banksiana Boreal 3 0.95a 30 <2 1 Yuan and Chen (2013)
mixed forest fire origin, Ontario, 1.55c
Canada
Populus tremuloides–Pinus banksiana Boreal 11 1.67a 30 <2 1 Yuan and Chen (2013)
mixed forest fire origin, Ontario, 3.08c
Canada
Populus tremuloides–Pinus banksiana Boreal 29 1.09a 30 <2 1 Yuan and Chen (2013)
mixed forest fire origin, Ontario, 2.11c
Canada
Populus tremuloides–Pinus banksiana Boreal 3 0.48a 30 <2 1 Yuan and Chen (2013)
mixed forest clear-cut origin, 0.87c
Ontario, Canada
Populus tremuloides–Pinus banksiana Boreal 11 0.65a 30 <2 1 Yuan and Chen (2013)
 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351 347

Appendix B (continued)
Site/location Biome Stand Fine-root Sampling Fine-root Study Reference
age production depth size duration
(year) (Mg ha!1 yr!1) (cm) (mm) (year)
mixed forest clear-cut origin, 1.68c
Ontario, Canada
Populus tremuloides–Pinus banksiana Boreal 29 1.35a 30 <2 1 Yuan and Chen (2013)
mixed forest clear-cut origin, 1.84c
Ontario, Canada
Fagus sylvatica–Quercus petrea Temperate 90– 1.47a 30 <2 1 Hertel and Leuschner
forests, Lüneburger Heide, 200 11.38c (2002)
Germany
Pinus sylvestris plantation, Boreal 37 3.35a 30 <2 3 Makkonen and
Ilomantsi, Finland 8.14c Helmisaari (1999)
Pinus sylvestris, Young stand, Boreal 18 1.39a 30 <2 1 Persson (1979)
Irantjärnsheden, Sweden 1.83c
Pinus sylvestris, Matured stand, Boreal 120 1.28a 30 <2 1 Persson (1979)
Irantjärnsheden, Sweden 1.59c
Larix principis–rupprechtii, Young Temperate 13 1.18a 30 <2 1 Wang et al. (2014)
plantation, Hebei province, China 0.87c
Larix principis–rupprechtii, Medium Temperate 22 1.38a 30 <2 1 Wang et al. (2014)
plantation, Hebei province, China 1.25c
Larix principis–rupprechtii, Matured Temperate 38 1.60a 30 <2 1 Wang et al. (2014)
plantation, Hebei province, China 1.34c
Eucalyptus grandis plantation Tropical 0.8– 2.26a 30 <2 1 Jourdan et al. (2008)
(Unfertilized), Itatinga, Brazil 1.3 1.28c
Eucalyptus grandis plantation Tropical 0.8– 2.16a 30 <2 1 Jourdan et al. (2008)
(fertilized), Itatinga, Brazil 1.3 0.84c
Cunninghamia lanceolata plantation, Subtropical 44 1.86a 30 62 2 Liu et al. (2014)
Hunan Province, China 0.86c
Acer saccharum, Ontario, Canada Boreal – 0.21a 40 <2 1 Pridoehl (2009)
0.80b 40
0.20c 50
Pinus sylvestris, Drained site 1, Boreal – 1.20a 20 <2 1 Finér and Laine (2000)
Lakkasuo, Finland 1.60c
Pinus sylvestris, Drained site 2, Boreal – 1.84a 20 <2 1 Finér and Laine (2000)
Lakkasuo, Finland 1.87c
Pinus sylvestris, Rääkkylä, Finland Boreal – 0.88a 20 <2 1 Finér and Laine (2000)
1.73c
Populus tremuloides monoculture Boreal – 0.60a 30 <2 1 Brassard et al. (2011b)
stand, Ontario, Canada 0.80c
Populus tremuloides–Picea mariana– Boreal – 1.00a 30 <2 1 Brassard et al. (2011b)
Abies balsamea mixed forests, 1.40c
Ontario, Canada
Populus tremuloides monoculture Boreal – 0.60a 30 <2 1 Brassard et al. (2011b)
stand, Québec, Canada 0.85c
Populus tremuloides–Picea mariana– Boreal – 0.95a 30 <2 1 Brassard et al. (2011b)
Abies balsamea mixed stands, 1.20c
Québec, Canada
Pinus banksiana monoculture stand, Boreal – 0.50a 30 <2 1 Brassard et al. (2013)
Ontario, Canada 1.50c
Populus tremuloides monoculture Boreal – 0.50a 30 <2 1 Brassard et al. (2013)
stand, Ontario, Canada 2.10c
Pinus banksiana–Picea glauca–Abies Boreal – 1.10a 30 <2 1 Brassard et al. (2013)
balsamea mixed stand, Ontario, 2.00c
Canada
Pinus banksiana–Populus tremuloides Boreal – 1.20a 30 <2 1 Brassard et al. (2013)
mixed stand, Ontario, Canada 2.30c
Lower montane forest, Chiriquí Tropical – 2.25a 28 <2 1 Adamek et al. (2011)
Province, Panama 3.24c 20
Betula platyphylla mixed stand, Temperate – 2.0a 30 <2 1.5 Sun et al. (2015)
Heilongjiang Province, China 2.6c
Methods: a = ingrowth-core; b = (mini) rhizotrons; c = sequential-coring.
348 S.D. Addo-Danso et al. / Forest Ecology and Management 359 (2016) 332–351

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