Plant Ecol

DOI 10.1007/s11258-016-0588-7

Root production in contrasting ecosystems: the impact

of rhizotron sampling frequency
Vasiliki G. Balogianni
Scott D. Wilson

. Gesche Blume-Werry .

Received: 27 October 2015 / Accepted: 11 March 2016

Springer Science+Business Media Dordrecht 2016

Abstract Despite their critical role in every terrestrial ecosystem, fine root production and mortality
have not been widely compared among systems due to
the practical difficulties of belowground research. We
examined fine root production and mortality among
five contrasting sites: native and invaded grassland in
eastern Montana, USA, aspen forest in southern
Saskatchewan, Canada, and birch forest and tundra
in northern Sweden. Additionally, we investigated the
importance of minirhizotron sampling interval on
measures of root production and mortality by comparing measures produced from 1-, 7-, 14-, and 21-day
sample intervals. Root length and mortality varied
significantly among sites, with invaded grassland
having the greatest root length ([2 9 than any other

Communicated by Prof. Lauchlan Fraser, Dr. Chris Lortie, and

Dr. JC Cahill.
V. G. Balogianni (&)
Departamento de Ecologia, Universidade Federal do Rio
Grande do Sul, Ave. Bento Goncalves 9500,
Porto Alegre Rio, Grande do Sul 91.501-970, Brazil
e-mail: vasiliki.balogianni@gmail.com
G. Blume-Werry
Department of Ecology and Environmental Science,
Climate Impacts Research Centre, Umea University,
981 07 Abisko, Sweden
S. D. Wilson
Department of Biology, University of Regina, 3737
Wascana Parkway, Regina, SK S4S 0A2, Canada

site) and significantly greater root mortality than

native grassland (54 %). In contrast, there were no
significant differences in root production among the
sites. Sample interval had no significant influence on
root production or mortality. Minirhizotron sampling
intervals up to 3 weeks did not underestimate the
measures of root production and mortality in comparison to measures derived from shorter sampling
intervals, regardless of the site studied. The results
suggest that 3 weeks can be an accurate and efficient
sample interval when studying root production and
mortality with minirhizotrons.
Keywords Arctic  Minirhizotrons  Mortality 
Prairie  Sample interval  Tundra

Introduction
Root systems comprise 1783 % of the plant mass in
ecosystems such as temperate forests and grasslands
(Mokany et al. 2006). Fine root dynamics, i.e.,
production and mortality, strongly influence soil
resources and nutrient cycling in many ecosystems,
including temperate grassland and forest (Partel and
Wilson 2002), dry heathland (Aerts et al. 1992),
savanna (West et al. 2004), and experimental grass
mixtures (Van Der Krift and Berendse 2002). For
example, nitrogen (N) input from root litter production
accounts for the 7187 % of the total N input in

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Plant Ecol

temperate forest and grassland (Steinaker and Wilson

2005). Notwithstanding their importance, fine root
production and mortality have not been studied as
extensively as their aboveground counterparts (Mariotte et al. 2013). This difference can be attributed to
the practical difficulties of belowground research that
demand a great amount of time and labor. Moreover, it
is difficult to separate plant root production from
mortality since those processes occur simultaneously
(Dubach and Russelle 1995). Here, we examine the
importance of sample frequency when studying root
dynamics in a time sequence by assessing root
production and mortality of several contrasting
ecosystems located in North America and Europe.
Differences among ecosystems in root production
and mortality are likely related to differences among
dominant growth forms (Jackson et al. 1996) and
climate (Vogt et al. 1995). However, only a few direct
comparisons of root dynamics among ecosystems
exist, yielding various and often contradicting results.
For example, replicated minirhizotron studies
revealed much less fine root length production and
mortality under a pine plantation than under native
pasture (Guo et al. 2007), but root production did not
differ between aspen forest and native grassland, and
root mortality was significantly greater beneath forest
(Partel and Wilson 2002). In contrast, fine root
productivity estimated using N budgets across a
forestgrassland continuum showed decreased fine
root production with increasing grass dominance
(Reich et al. 2001).
Minirhizotrons are especially suitable for measuring root production and mortality, since they allow
repeated non-destructive sampling of identical locations without continuous soil disturbance, and enable
direct monitoring of specific root segments from birth
to death (Johnson et al. 2001; Majdi et al. 2005; Peek
2007). In addition, minirhizotrons detect up to 40 %
more fine roots than do harvest methods (Hendricks
et al. 2006). An important consideration when measuring fine root production and mortality with minirhizotrons is the selection of a suitable interval between
two consecutive sampling events. In practice, sample
interval selection comprises a tradeoff between measurement accuracy and the time and resources available for collecting images and extracting data
(Johnson et al. 2001). However, it is crucial to select
a sample interval that accounts for the potentially high
rate of root appearances and disappearances occurring

123

between two consecutive sampling events in order to

avoid underestimating root production and mortality
(Johnson et al. 2001). Minirhizotron experiments have
shown that 8- and 4-week sample intervals greatly
underestimate root production and mortality relative
to a 2-week interval in tree seedlings planted at a field
site (Johnson et al. 2001), 4-week sample intervals
underestimate production and mortality relative to a
1-week interval in woodland (Stevens et al. 2002), an
8-week sample interval underestimates production and
mortality relative to a half-week interval in tree stands
(Tingey et al. 2003), and 4-week sample intervals
underestimate production and mortality relative to a
half-week interval in upland grassland (Stewart and
Frank 2008). Indeed, most published studies use
sample intervals less than four weeks, but only a few
studies use intervals less than 2 weeks (Zobel 2003;
McCormack et al. 2015). However, even a two-week
sample interval can underestimate the production and
mortality in some systems. For example, lateral fine
roots in maize fields have a life span of only 2 weeks
(Cahn et al. 1989). Thus, roots could appear and
disappear between two sampling events and be
completely missed. Similarly, two-week sample intervals greatly underestimated root production and
mortality relative to one-week intervals in legume
crops (Dubach and Russelle 1995). Finally, no direct
comparisons among short sample intervals are found
in the literature, while the shortest sample interval
studied was 3 days (Stewart and Frank 2008; Tingey
et al. 2003). Thus, investigating the effect of sample
interval on fine root dynamics measures by comparing
long and short intervals is of a great interest.
Because minirhizotrons are used in contrasting
ecosystems such as grasslands and forests (Johnson
et al. 2001), it is important to know if the effect of
sample interval varies among ecosystems. Thus, we
studied the root length, root production, and mortality
in five contrasting ecosystems and we aimed to
determine the effect of sample frequency on measures
of fine root production and mortality.

Methods
Study areas
We studied five sites (Table 1) comprising native
mixed-grass prairie in Montana, a nearby stand

Plant Ecol
Table 1 Description of studied sites
Site

Cl

Location

Latitude

Longitude

Al

Dominant species

Invaded
grassland

Temp

Medicine
Lake, USA

48280 1600 N

104220 1600 W

600

4.9a

340a

Agropyron cristatum

Native
grassland

Temp

48280 1600 N

104220 1600 W

600

4.9a

340a

Bouteloua gracilis, Pascopyrum

smithii, Selaginella densa

Tundra

Arc

Medicine
Lake, USA
Karkevagge,
Sweden

68230 000 N

18200 3500 E

740

-3d

1180d

Carex bigelowii, Salix polaris, mosses

Aspen
forest

Temp

White Butte,
Canada

50460 0700 N

10430 6800 W

620

2.3b

378b

Populus tremuloides, Symphoricarpos

occidentalis, Rubus idaeus

Birch
forest

Arc

Nissonjohkke,
Sweden

68190 5100 N

18450 3300 E

400

-0.1c

335c

Betula pubescens ssp. czerepanovii,

Deschampsia flexuosa, Empetrum
nigrum

Cl climatic zone, Al altitude (m), T mean annual temperature (C), P mean annual precipitation (mm), Temp temperate ecosystems,
Arc arctic ecosystem
a

For 19112013. Source: http://www.wrcc.dri.edu/

For 19712000. Source: http://climate.weather.gc.ca

For 19812010. Source: Abisko scientific research station

For 20062011. Source: http://luftwebb.smhi.se/

dominated by the Eurasian invasive grass Agropyron

cristatum (Balogianni et al. 2015), arctic tundra in
northern Sweden (Veen et al. 2015), aspen forest in
Saskatchewan (Steinaker and Wilson 2005), and birch
forest in northern Sweden (Veen et al. 2015). In each
site, five transparent cellulose acetate butyrate
minirhizotron tubes (180 cm long, 5 cm internal
diameter) were installed at 45 to the soil surface at
the dates given in Table 2. Tubes were separated by at
least 10 m and were arrayed across 210 ha in each
site. Tubes were installed at least two years before data
collection, allowing roots time to colonize the
minirhizotron tube surface.
Root measurements
Roots were sampled in early summer for the Montana
sites, mid-summer for Saskatchewan aspen forest, and
late summer for the Swedish sites, all in 2012 (Table 2).
Sampling periods occurred near the time of maximum
Table 2 Periods of
minirhizotron installation
and image collection at
each site

root production for each site (Milchunas and Lauenroth

1992; Stewart and Frank 2008 for North American
semi-arid grasslands; Steinaker et al. 2010 for the aspen
forest; Blume-Werry et al. 2016; Sloan et al. 2016 for
the Swedish sites). Images (18 9 14 mm) each were
collected 0, 4, 7, 11, 14, 18, 22, 25, 29, and 32 cm from
the soil surface inside the minirhizotron tube using a
digital camera (Bartz Technology, USA) and an
indexing handle system which allowed precise relocation of the camera every sampling time. This depth
range contains the bulk of roots (Steinaker and Wilson
2005). Root images were collected every day for 5 days
(i.e., on days 15) and on day 8, day 15, and day 22. Due
to a technical failure, we collected images from the
aspen forest only during days 18.
Image and data analysis
Root images were analyzed using WinRHIZOTRON
MF 2007 software (Regent Instruments Inc., Canada).

Site

Minirhizotron installation

Image collection

Invaded grassland

Spring 2006

MayJune 2012

Native grassland

Spring 2006

MayJune 2012

Tundra

Spring 2010

AugustSeptember 2012

Aspen forest

Summer 2000

August 2012

Birch forest

Spring 2010

AugustSeptember 2012

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Plant Ecol

For each sampling date, we traced the length of all live

roots in each image. Root length per tube was
calculated as the average of all images [meters of root
length per square meter of examined tube surface area
(m m-2)].
Root production was defined as the sum of the length
of new roots formed and any increase in length of
existing roots since the previous sampling day (Johnson et al. 2001). Root mortality was defined as the sum
of the length of roots that had disappeared and any
decrease in length of existing roots since the previous
sampling day. Root production and mortality for each
interval was expressed as the average meters of root
length that appeared or disappeared per square meter
image area per day (m m-2 days-1) in each tube.
Statistical analysis
We analyzed root length using repeated measures
analysis of variance (rmANOVA) with site as the
main effect. Tukeys tests were used to compare
means among ecosystems and time. To test the
difference in root length between temperate and
arctic sites, we used planned comparisons. We
compared root production and mortality among sites
and sample intervals using weighted ANOVAs, with
weights assigned to intervals based on how often they
were included. Thus, the 1-day interval was weighted
4, the 7-day interval was weighted 3, and the 14- and
21-day intervals were weighted 1. Tukeys tests were
used to compare means among sites and sample
intervals. Means from the aspen forest for days 18
are reported, but this site was used only in the
statistical analysis of root length. Additionally, we
analyzed root production and mortality with the use
of linear mixed effect models and the analysis
produced similar results to weighted ANOVAs (data
not shown). All statistical analyses were performed
using JMP 10.0. To help stabilize the variance, all
data were fourth-root transformed.

Results
Root length
Root length varied significantly among sites
(P \ 0.0001). Invaded grassland had root length
significantly greater than any other site (Fig. 1) and

123

temperate sites had significantly greater root length

than arctic sites (P \ 0.0001, Fig. 1). Total root length
increased significantly with time (P = 0.009, Fig. 2),
with significantly more root having been measured in
days 4, 5, and 8 in comparison to day 1. No significant
interaction between site and time was observed
(P = 0.76, Fig. 2).
Root production and mortality
Root production did not vary significantly among
sites, sample intervals (Fig. 3), or their interaction,
despite the relatively high P value (P = 0.1) that was
observed for the interaction (Table 3). Root mortality
varied significantly among sites (P \ 0.001, Table 3).
Root mortality in birch forest and in invaded grassland
was significantly greater than root mortality in native
grassland and tundra, which was zero (Fig. 4). Root
mortality did not vary significantly among sample
intervals (Fig. 3), or the interaction between site and
sample interval.

Discussion
Variation in root length revealed two major trends.
First, root length beneath the invasive grass A.
cristatum was more than twice that of any other site
studied, including the nearby native grassland. Other
studies also found increased root length after invasion
by the same species, A. cristatum (MacDougall and
Wilson 2011; Balogianni et al. 2015). Second, climate
and the accompanying differences in dominant plant
growth forms appear to have a strong effect on root
length. For example, root length was 56 % greater in
the temperate aspen forest than arctic birch forest.
Additionally, the 71 % greater root length found in
temperate native grassland compared with herbaceous
tundra also corresponds to temperature differences
(Table 1). Thus, the greater root length found in
temperate site may be associated with the sites higher
temperature which tends to increase evaporation and
decrease soil water. As a general trend, plants allocate
more growth to roots as water becomes scarce (King
et al. 1999; Tierney and Fahey 2002; Steinaker et al.
2010). On the other hand, it is possible that shorter
growing seasons in the Arctic also limited the extent to
which roots colonized the surfaces of the rhizotron
tubes.

Plant Ecol
Fig. 1 Mean (SE) root
length (m m-2) in five sites,
averaged across eight
sampling days (N = 5).
Different uppercase letters
represent significant
(P \ 0.05) differences
among sites as revealed by
repeated measures ANOVA
followed by Tukeys tests

The increase of root length over time (7 % over

22 days, Fig. 2) reflects the fact that root production
exceeded mortality during the study period at every site
studied, regardless of the sampling interval (Fig. 3).
Root growth occurs throughout our sampling period
(Steinaker et al. 2010; Blume-Werry et al. 2016).
However, if the colonization of the minirhizotron tube
surface has not reached equilibrium, we also expect
fine root production to be greater than mortality (Joslin
and Wolfe 1999; Burton et al. 2000). Indeed, previous
studies report that root colonization following minirhizotron installation can last up to eight years (Aerts et al.
1989; Hendrick and Pregitzer 1996; Burton et al. 2000;
Balogianni et al. 2014). Differences in rates of root
colonization might affect comparisons of root length
between contrasting sites especially because the year
of tube installation varied greatly among sites (tubes
were 212 years old), even though root production was
similar in every site. Similarly, a recent study in
invaded and native grasslands did not detect any
significant interaction between the time after tube
installation and the study system when measuring root
length (Balogianni et al. 2014), suggesting that colonization of the tube surface is not likely a constraint for
comparing root length among sites. Thus, seasonal
dynamics of root growth may have exerted stronger
effects on the length increase than did the colonization
by roots of the minirhizotron surface.

In general, our measures of root production and

mortality are similar to previous values from minirhizotron studies (Burton et al. 2000; Stewart and Frank
2008). We did not detect significant differences in root
production among the sites, which may indicate that root
production is more dependent on season than site. This
result echoes the findings of a previous study in which
root production in a temperate aspen forest was similar to
that in native grassland, and was related more to seasonal
dynamics than vegetation type (Partel and Wilson 2002).
On the other hand, the P value for the interaction term
between site and sample interval was 0.1 for root
production (Table 3), raising the possibility that
increased numbers of sites or sample intervals might
find a significant interaction. Moreover, our result of
significantly greater root mortality in birch forest than
native grassland is also in agreement with the aforementioned study, where roots live nearly twice as long in
grassland as in forest (Partel and Wilson 2002). In
contrast, other works report less root mortality and
longer fine root lifespan for trees than grasses (Guo et al.
2007; Chen and Brassard 2013), while other studies have
reported that fine root mortality was similar between
grasslands and forests and was more influenced by the
nutrients status of the soil (Pinno and Wilson 2013).
The relevance of these results for other locations,
ecosystems, and years remains to be determined. The
timing of maximum root productivity, for example, can

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Plant Ecol

Fig. 2 Mean (SE) root length (m m-2) in five sites over eight sampling days and in aspen forest over six sampling days

vary between years by a matter of weeks (Blume-Werry

et al. 2016). Further, we studied the root dynamics at
only one time during the growing season, with this time
varying at every site (Table 2), and a consideration of
several complete comparable growing seasons would
give a clearer picture of the effect of sampling frequency
on the accuracy of root production measurements.

123

Similarly, we sampled only five locations to represent

each ecosystem, and more general insights would
certainly result from incorporating more locations.
Overall, our results do not support the possibility
that longer sample intervals significantly underestimate root production and mortality, relative to measurements derived from shorter sample intervals

Plant Ecol
Fig. 3 Mean (SE) root
production (a) and mortality
(b) (m m-2 day-1) derived
from 1-, 7-, 14-, and 21-day
sample intervals, averaged
across four ecosystems.
Aspen forest was not
included in the analysis and
in the graph due to missing
data

Table 3 Weighted ANOVA results for root production and mortality with site and sample interval as the main factors, and their
interactions
Source of variation

Root production

Root mortality

DF

F ratio

DF

F ratio

Site

0.45

0.72

7.46

\.001

Sample interval

0.05

0.98

0.41

0.74

Site * sample interval

1.42

0.1

0.15

Only four of the five sites were included

(Johnson et al. 2001; Stevens et al. 2002; Tingey et al.

2003; Stewart and Frank 2008). The 1-day sample
interval measured much greater root production than
the rest of the sample intervals (68, 59, and 71 % for
the 7-, 14-, and 21-day sample intervals, respectively),

but this difference was not statistically significant,

perhaps due to large variation. Additionally, root
production measurements in the 1-day sample interval
may not have been as accurate as those in longer
intervals, which estimated production averaged over

123

Plant Ecol
Fig. 4 Mean (SE) root
mortality (m m-2 day-1) in
four ecosystems, averaged
across sample intervals.
Different uppercase letters
represent significant
differences between sample
intervals (P \ 0.05) within
each ecosystem. Aspen
forest was not included in
the analysis due to missing
data

several days. Further, given the very small sampling

area, the error of repositioning the camera might be
larger than the root production that occurred in only a
single day. Overall, taking into account the resource
and labor demands of short sample intervals, combined with the lack of significant effects that sample
interval had on measures of root production and
mortality, we suggest that longer sample intervals,
such as 21 days, provide a reasonable compromise
between research efficiency and accuracy when comparing contrasting ecosystems.
Acknowledgments We thank D. Sandbeck and S. Trager for
practical help, Medicine Lake National Wildlife Refuge and the
Abisko Scientific Research Station for access and logistical
support, reviewers for helpful suggestions, and the Natural
Sciences and Engineering Research Council of Canada for
funding.

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