Size Dependency of Post-Disturbance Recovery of Multi- Stemmed Resprouting Trees

Abstract

In frequently burned ecosystems, many plants persist by repeated resprouting from basal or belowground buds. This strategy requires that plants reach a balance between biomass loss and recovery, which depends on the shape of the relationship between pre- and post-fire size. Previous analyses of this relationship, however, have focused on the size of the largest stem, which ignores the importance of the multi-stem growth habit that is common in pyrogenic ecosystems. We hypothesized that the presence of multiple stems causes a substantial shift in the relationship between pre- and post-fire size and in the relationship between pre-fire size and size recovery. We measured the height and basal diameter, then calculated volume and biomass, of all stems of six tree species before and nine months after complete removal of aboveground biomass via coppicing. The number of resprouts was correlated with the original number of stems for four species. For all species, the relationship between pre-coppicing and resprout size fit a positive curvilinear function, and the shape of this curve did not differ for maximum and total stem size. Smaller individuals recovered a larger proportion of their pre-coppicing size than larger individuals, but the shape of the size recovery curves were the same regardless of whether the analysis was performed with all stems or only the largest stem. Our results indicate that measuring only the largest stem of multi-stemmed individuals is sufficient to assess the ability of individuals to recover after complete loss of aboveground biomass and persist under frequent burning.

Full text

Size Dependency of Post-Disturbance Recovery of Multi-
Stemmed Resprouting Trees
Jennifer L. Schafer*
¤
, Michael G. Just
Department of Plant and Microbial Biology, North Carolina State University, Raleigh, North Carolina, United States of America
Abstract
In frequently burned ecosystems, many plants persist by repeated resprouting from basal or belowground buds. This
strategy requires that plants reach a balance between biomass loss and recovery, which depends on the shape of the
relationship between pre- and post-fire size. Previous analyses of this relationship, however, have focused on the size of the
largest stem, which ignores the importance of the multi-stem growth habit that is common in pyrogenic ecosystems. We
hypothesized that the presence of multiple stems causes a substantial shift in the relationship between pre- and post-fire
size and in the relationship between pre-fire size and size recovery. We measured the height and basal diameter, then
calculated volume and biomass, of all stems of six tree species before and nine months after complete removal of
aboveground biomass via coppicing. The number of resprouts was correlated with the original number of stems for four
species. For all species, the relationship between pre-coppicing and resprout size fit a positive curvilinear function, and the
shape of this curve did not differ for maximum and total stem size. Smaller individuals recovered a larger proportion of their
pre-coppicing size than larger individuals, but the shape of the size recovery curves were the same regardless of whether
the analysis was performed with all stems or only the largest stem. Our results indicate that measuring only the largest stem
of multi-stemmed individuals is sufficient to assess the ability of individuals to recover after complete loss of aboveground
biomass and persist under frequent burning.
Citation: Schafer JL, Just MG (2014) Size Dependency of Post-Disturbance Recovery of Multi-Stemmed Resprouting Trees. PLoS ONE 9(8): e105600. doi:10.1371/
journal.pone.0105600
Editor: Christopher Carcaillet, Ecole Pratique des Hautes Etudes, France
Received May 4, 2014; Accepted July 25, 2014; Published August 21, 2014
Copyright: ß2014 Schafer, Just. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its
Supporting Information files.
Funding: This research was supported by a cooperative agreement between the US Army Engineer Research and Development Center and North Carolina State
University (W9132T-11-2-0007 to W. Hoffmann). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the
manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* Email: schaferj@william.jewell.edu
¤ Current address: Department of Biology, William Jewell College, Liberty, Missouri, United States of America
Introduction
Resprouting provides resilience to fire and allows plants to
persist in pyrogenic ecosystems. When aboveground stems are
killed by fire (i.e., topkilled), species that are able to resprout
generate new biomass from plant parts that survive fire [1,2] such
as basal buds, lignotubers, rhizomes, or the root collar [3,4].
Resprouting ability and resprout biomass [5–7] are influenced by
the size of the belowground bud bank [8], the pool of belowground
resources (e.g., carbohydrates and nutrients [9–14]), and pre-fire
plant size [15,16].
In frequently burned ecosystems, resprouting species are
subjected to repeated cycles of topkill and resprouting [17], so
persistence depends on the ability of plants to recover their pre-fire
size to maintain a balance between biomass loss and recovery
[13,18]. Resprout height and diameter are positively correlated
with pre-fire stem height and diameter [16,19,20], with the
relationship between pre- and post-fire size fitting a curvilinear
scaling function [18]. This ‘‘resprout curve’’ illustrates the balance
between biomass loss and recovery and determines the equilibrium
size (i.e., where pre-fire and post-fire size are equal) upon which
plants will converge over multiple fire cycles ([18]; Figure 1A).
Although resprout size is correlated with pre-fire size [16,19,20],
large plants often recover their pre-fire size more slowly than small
plants [18,21]. This ‘‘recovery curve’’ is a negative curvilinear
relationship between pre-fire size and the ratio of post- to pre-fire
size (Figure 1B).
Studies on the relationship between pre- and post-fire size and
the size dependency of post-fire recovery, however, often focus
only on the largest pre-fire stem and largest resprout [16,18,19]
even though many resprouting species are multi-stemmed before
and/or after fire (e.g., [22–24]). In fact, the number of resprouts is
correlated with the number of stems pre-fire [20,25,26]. Allocation
of biomass to multiple stems, rather than one stem, may be
beneficial due to limitations on maximum stem height and growth
rates [27–29] and the improvement in competitive success
conferred by a large crown volume [30]. If the curvilinear nature
of resprout and recovery curves is a consequence of limitations on
maximum stem growth rates [28,31], then this limitation could be
overcome by producing multiple stems.
Accounting for all stems of multi-stemmed resprouting species,
therefore, may cause an upward shift in resprout (Figure 1A) and
recovery (Figure 1B) curves. An upward shift in the resprout curve
would indicate that individual plants are able to maintain a greater
biomass (i.e., a greater equilibrium plant size) with frequent
burning. Consequently, larger individuals would be able to recover
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their pre-fire size. In this case, production of multiple stems could
increase the ability of plants to escape a suppressed state of
repeated topkill and resprouting [17,32,33] during a longer fire
free interval. Alternatively, accounting for all stems could lead to a
change from a curvilinear to linear relationship between pre- and
post-fire size and size recovery, indicating that curvilinearity is not
a fundamental property of resprouting. Regardless, understanding
the impact of multiple stems on resprout and recovery curves is
important because the ability of individual plants to recover
biomass lost during fire allows for persistence with repeated
burning [13].
We assessed resprouting success and the size dependency of
volume and biomass recovery after complete loss of aboveground
biomass. Specifically, we coppiced aboveground stems – as has
been done in other studies to simulate fire-induced topkill
[6,14,34,35] – of six tree species that occur in the pyrogenic
longleaf pine savannas and adjacent stream-head pocosins of the
southeastern United States [36,37]. To test the hypothesis that
accounting for all stems of multi-stemmed resprouting species
causes a shift in resprout and recovery curves, we measured all
stems pre-coppicing and all resprouts. We assessed possible shifts
in resprout and recovery curves by testing for differences in the
slopes and y-intercepts of the log-transformed relationships
between pre-coppicing and resprout size (i.e., volume and biomass)
of the largest stem (maximum size) and all stems (total size;
Figures 1C and 1D).
Materials and Methods
Ethics Statement
We obtained approval for data collection from the Endangered
Species Branch at Fort Bragg Military Installation. Data was
collected on publicly owned land. No protected species were used
in this study.
Study site and species
We conducted our study at Fort Bragg, which is located in the
Sandhills region of North Carolina (35u079N, 79u109W).
Longleaf pine (Pinus palustris Mill.) savanna (e.g., upland pine/
scrub oak sandhill sensu [36]) is the most widespread vegetation
type on the installation. Pine needles and wiregrass (Aristida stricta
Michx.) accumulate quickly and facilitate frequent fire; the
average historical fire return interval is approximately 2 years
[38]. For the lowland stream-head pocosins (i.e., wetlands)
Figure 1. Hypothesized shifts in resprout and recovery curves resulting from inclusion of all stems. (A) Differences in resprout curves
that could arise from inclusion of all stems of multi-stemmed trees. Stars indicate the equilibrium size that develops over multiple fire cycles that
corresponds to the point at which biomass loss is equal to biomass recovery (i.e., intersects with the 1:1 line; following [18]). (B) Recovery curves that
correspond with resprout curves. (C) Illustration of the transformation of resprout curves to a logarithmic scale. (D) Illustration of the transformation
of recovery curves to a logarithmic scale. We assessed shifts in resprout and recovery curves by testing for differences in the slopes and y-intercepts
of the log
10
-transformed relationships between maximum and total size and size recovery.
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embedded within the savanna matrix [37], higher moisture
content and differences in species composition contribute to a
longer fire return interval of 7–50 years [39]. Soil moisture
increases along the gradient from upland savanna to lowland
pocosin, and soils are classified as entisols, inceptosols, or ultisols
[40]. Mean annual precipitation is 1275 mm, and summer is the
wettest season [37]. Fort Bragg is divided into discrete landscape
units locally referred to as burn blocks, within which prescribed
fire is applied approximately every 3 years [41]. Prescribed fires at
Fort Bragg are conducted during the dormant season (December–
March) and the growing season (April–July) [42]. Lightning
Table 1. General characteristics of individuals included in the study.
Species
a
#Individuals
Coppiced
b
#Individuals
Resprouted
#of Stems Pre-
Coppicing #of Resprouts
Maximum Stem
Height (cm)
c
Maximum Basal
Diameter (mm)
c
Quercus laevis 29 26 1–6 0–8 60–330 6.99–61.18
Diospyros virginiana 26 26 1–2 1–5 58–285 7.74–40.01
Liquidambar styraciflua 32 31 1–5 0–17 12–399 2.38–41.20
Liriodendron tulipifera 29 27 1–8 0–37 37–610 5.12–56.92
Persea palustris 31 31 1–4 1–7 53–289 5.46–34.33
Acer rubrum 30 28 1–6 0–9 38–382 4.27–30.13
a
Species are listed in order of their position along the savanna-to-pocosin gradient.
b
Does not include individuals burned in the June 2013 wildfire.
c
For stems pre-coppicing.
doi:10.1371/journal.pone.0105600.t001
Figure 2. Ratio of resprout stem number to pre-coppicing stem number. In the boxplots, the solid and dotted bars represent the median
and mean, respectively; the lower and upper bars represent the 25
th
and 75
th
percentiles, respectively. The lower and upper ‘‘whiskers’’ show the
largest and smallest values that are not outliers and the lower and upper dots show the 5
th
and 95
th
percentiles. Kruskal-Wallis
X
2
= 20.03, P= 0.001;
different letters indicate significant differences among species. The dashed line indicates where the number of resprouts equals the number of stems
pre-coppicing.
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ignited fires in the southeastern US typically occur during the
spring and summer (April–September) [43,44].
We selected six focal species that differ in their distribution
along the savanna-to-pocosin gradient: Quercus laevis Walter
(turkey oak), Diospyros virginiana L. (persimmon), Liquidambar
styraciflua L. (sweetgum), Liriodendron tulipifera L. (tulip poplar),
Persea palustris (Raf.) Sarg. (swamp bay), and Acer rubrum L. (red
maple; Table 1; nomenclature follows The PLANTS Database
(US Department of Agriculture, Natural Resources Conservation
Service; http://plants.usda.gov/java/). Quercus laevis is a savan-
na species, and D. virginiana occurs in the savanna and the
ecotone between savanna and pocosin. Liquidambar styraciflua is
most common in the ecotone, and L. tulipifera,P. palustris, and
A. rubrum are restricted to the pocosin and ecotone. All study
species typically resprout from basal or belowground buds after
topkill via fire or other damage.
Figure 3. Curvilinear relationships between total pre-coppicing stem volume and total resprout stem volume.
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Figure 4. Curvilinear relationships between total pre-coppicing stem biomass and total resprout biomass.
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Field measurements and calculations
In October 2012, we selected 30–32 individuals of each species
that spanned a range of maximum stem heights and diameters
(Table 1); even the largest individuals were considered saplings.
Individuals were found throughout their distribution along the
savanna-to-pocosin gradient in multiple burn blocks (n = 6) that
were burned 3–4 years previously. We measured the height and
basal diameter (within 2 cm of ground level) of all stems of each
individual and then, to simulate topkill, coppiced all stems at
,2 cm above ground level. Stems were coppiced in October, at
the beginning of the dormant season and after the typical wildfire
season [43,44]. Coppicing is commonly used as a surrogate for
disturbance-induced topkill (e.g., [34,35]), and resprouting success
is similar between burned and coppiced individuals [6,15,45]. A
wildfire in June 2013 burned a small section of one of our study
sites, which reduced our sample size of all species except L.
styraciflua (Table 1). In July 2013, 9 months after coppicing and
near the end of the growing season, we measured the height and
basal diameter of all resprouts of each individual.
For individuals that resprouted, we calculated the conical
volume of each stem from measurements of stem height and
diameter. We determined the maximum stem volume (i.e., volume
of the largest stem) and total stem volume (i.e., the sum of volumes
of all stems) of each individual pre-coppicing and after resprouting.
For three species – Q. laevis,D. virginiana, and L. styraciflua –we
used allometric equations from Robertson and Ostertag [46] to
calculate maximum and total stem biomass of each individual pre-
coppicing and after resprouting. Except for large pre-coppiced Q.
laevis and small L. styraciflua resprouts, the majority of our stems
were within the range of diameters used to develop the allometric
equations [46].
Statistical analyses
For each species, we analyzed the relationship between pre-
coppicing stem number and the number of resprouts using
Kendall’s tau. To analyze differences among species in resprouting
success (i.e., production of resprouts), we calculated the ratio of
resprouts to pre-coppicing stems for all individuals and used a
Kruskal-Wallis test, with post-hoc pair-wise significance tests
Figure 5. Relationships between pre-coppicing stem volume and resprout stem volume on a logarithmic scale. Total stem volume is
denoted with filled symbols and dashed lines. Maximum stem volume is denoted with open symbols and solid lines. ** P,0.01, *** P,0.001 for
regressions. Pvalues for differences in slopes and intercepts between maximum and total volume are given.
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adjusted for multiple comparisons. To determine if there was a
significant curvilinear relationship between total resprout size and
total pre-coppicing size, we used the curve estimation function in
SPSS version 19.0 (IBM Corporation, Armonk, NY, USA).
Specifically, we fit power functions to the relationships between
total pre-coppicing stem volume and total resprout stem volume
(for all species) and total pre-coppicing stem biomass and total
resprout biomass (for Q. laevis,D. virginiana, and L. styraciflua).
We used a regression model with log
10
resprout size (i.e., volume
or biomass) as the dependent variable and log
10
pre-coppicing size
(i.e., volume or biomass), data type (i.e., maximum or total size,
coded as 1 and 0, respectively), and an interaction term (log
10
pre-
coppicing size * data type) as independent variables entered into
the model to determine if there was a significant difference
between the slopes and y-intercepts of the relationships between:
(1) pre-coppicing and resprout maximum and total stem size
(Figure 1C) and (2) pre-coppicing size and recovery of maximum
and total stem size (Figure 1D) for each species.
Results
For all species, at least 90% of individuals resprouted after
coppicing (Table 1). The number of resprouts was positively
correlated with the number of coppiced stems for Q. laevis
(t= 0.339, P= 0.025), L. styraciflua (t= 0.296, P= 0.042), P.
palustris (t= 0.296, P= 0.058), and A. rubrum (t= 0.491,
P= 0.001). The number of resprouts of D. virginiana (t= 0.251,
P= 0.239) and L. tulipifera (t= 0.224, P= 0.139) was not
correlated with the number of coppiced stems. The number of
Figure 6. Relationships between pre-coppicing stem biomass and resprout stem biomass on a logarithmic scale. Total stem biomass is
denoted with filled symbols and dashed lines. Maximum stem biomass is denoted with open symbols and solid lines. ** P,0.01, *** P,0.001 for
regressions. Pvalues for differences in slopes and intercepts between maximum and total biomass are given.
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Figure 7. Relationships between pre-coppicing stem volume and the ratio of resprout volume to pre-coppicing volume. Data is
shown on a logarithmic scale. Total stem volume is denoted with filled symbols and dashed lines. Maximum stem volume is denoted with open
symbols and solid lines. * P,0.05, ** P,0.01, *** P,0.001 for regressions; NS indicates not significant. Pvalues for differences in slopes and intercepts
between maximum and total volume are given.
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resprouts of all species tended to be equal to or greater than the
number of coppiced stems (Figure 2); 73% of individuals that
resprouted had more resprouts than coppiced stems.
There was a positive curvilinear relationship between total
resprout and pre-coppicing stem volume (Figure 3) and biomass
(Figure 4) for all species studied. There was no difference between
the slopes or intercepts of the relationships between pre-coppicing
and resprout maximum and total volume (Figure 5) and pre-
coppicing and resprout maximum and total biomass (Figure 6). In
other words, for all species, resprout curves were similar for
maximum and total size.
Recovery of volume and biomass was negatively correlated with
pre-coppicing volume and biomass, regardless of whether all stems
were included in the analysis. For all species, there was no
difference between the slopes or intercepts of the relationships
between recovery of maximum and total volume (Figure 7) and
recovery of maximum and total biomass (Figure 8). Most
individuals recovered less than 55% of their maximum stem
volume.
Discussion
The ability of plants to resprout after topkill contributes to their
persistence in pyrogenic ecosystems. Across species in our study,
95% of individuals resprouted after complete removal of
aboveground biomass (Table 1). Resprout number has been
found to be positively correlated with the number of stems present
before fire [20]; this was the case for four of our six study species.
Individuals with more stems pre-fire may have larger storage
organs, which translate to larger pools of carbohydrates and buds
to support resprouting [7,47,48]. For the two species in our study
for which resprout number was not positively correlated with pre-
coppicing stem number, D. virginiana and L. tulipifera,
individuals with only one stem pre-coppicing produced 1 to 5
and 1 to 14 resprouts, respectively. Factors such as bud activation
and proximity of buds to the soil surface [49], as well as pre-fire
stem size [15,16], may have affected resprout number.
We found that total resprout size was positively correlated with
pre-coppicing total size and fit a curvilinear function (Figures 3
and 4). Although maximum resprout size may be limited by
growth rates [28,31], the ability to increase mechanical strength to
support height growth [50], or physiological changes that alter
allocation of photosynthates [51], we found no difference in the
resprout curves for maximum and total size (Figures 5 and 6;
determined by analyzing log
10
-transformed data). Accounting for
all stems did not cause a significant shift in the resprout curves, and
thus, production of multiple stems does not change the size at
which individuals persist in frequently burned ecosystems. One
explanation for the lack of upward shift in resprout curves could be
related to the concomitant increase in resprout and pre-coppicing
volume and/or biomass – individuals in our study had up to eight
stems pre-coppicing – such that inclusion of all stems of multi-
stemmed individuals affected the location of an individual on the
curve rather than the shape of the curve. In addition, intraspecific
variation in pre- and post-fire sizes could be related to resource
availability because plants in high-resource environments are
larger after fire than plants of the same initial size in low-resource
environments [18].
Similar to Grady and Hoffmann [18], when we accounted for
only the largest stem, larger individuals recovered a smaller
fraction of their pre-coppicing size than smaller individuals.
Contrary to our hypothesis, there was no difference in the shape of
the recovery curves of maximum and total size (Figures 7 and 8;
determined by analyzing log
10
-transformed data). Accounting for
all stems, rather than only the largest stem, does not affect which
individuals, in terms of pre-coppicing size, are able to recover all
biomass lost during fire. Although 73% of the resprouting
individuals in our study experienced an increase in stem number
after complete removal of aboveground biomass (Figure 2), our
results suggest that the potential benefits of producing multiple
stems do not extend to post-disturbance biomass recovery.
The shape of resprout and recovery curves may be influenced
by resprout age. Historically, the fire return interval in longleaf
pine savannas ranged from 0.5 to 12 years [38], and savannas at
our study site are currently burned every 3 years, on average, with
stream-head pocosins generally burning less frequently [39]. The
number of resprouts per clump is higher in more recently burned
sites than longer unburned sites [52,53], suggesting that self-
thinning of resprouts can occur over time such that total size may
converge on maximum size as the number of stems decreases.
Furthermore, large individuals recovered a lower proportion of
their size regardless of whether resprouts were 9 months (Figures 7
and 8) or 3 years old [18].
The shape of resprout and recovery curves may also be
influenced by fire season. In the southeastern US, plants burned
during the dormant season have greater post-fire stem densities
[4,54] and aboveground biomass [55] than plants burned during
the growing season. Differences in resprout number should have
little or no effect on the persistence equilibrium since there is no
difference between resprout and recovery curves of maximum and
total stem size (Figures 5-8). Greater biomass [55] and a larger
increase in growth rates [56] after dormant season fires suggests
that resprout curves of plants burned during the dormant season
could be shifted upward from plants burned during the growing
season. Nonetheless, any effects of fire season on resprout and
recovery curves should be consistent for maximum and total stem
size.
Our study assessed the importance of considering all stems, not
just the largest stems, when assessing size recovery after complete
removal of aboveground biomass. The ability of plants to produce
multiple resprouts did not allow individuals to reach a larger
equilibrium size or recover a greater proportion of their pre-
coppicing size. Production of multiple stems, therefore, does not
appear to affect persistence in frequently burned ecosystems in
regard to the balance between biomass loss and recovery. Our
study species are all trees that resprouted from the root crown; it is
not clear how differences in allometric constraints on resprout
allocation (e.g., shrubs vs. trees; [57]) or the belowground structure
from which resprouts are produced (e.g., lignotubers or rhizomes;
[3]) influence relationships between maximum and total stem size.
Nevertheless, accounting for only the largest pre-fire stem and
largest resprout appears to be an adequate predictor of species’
equilibrium size and their ability to recovery their pre-fire size and
Figure 8. Relationships between pre-coppicing stem biomass and the ratio of resprout biomass to pre-coppicing biomass. Data is
shown on a logarithmic scale. Total stem biomass is denoted with filled symbols and dashed lines. Maximum stem biomass is denoted with open
symbols and solid lines. ** P,0.01, *** P,0.001 for regressions. Pvalues for differences in slopes and intercepts between maximum and total biomass
are given.
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should not lead to misinterpretation of persistence ability over
multiple fire cycles.
Supporting Information
Dataset S1 Pre-coppicing and resprout stem volume
and biomass.
(XLSX)
Acknowledgments
We thank Alicia Ballard, Spencer Bell, Bradley Breslow, and Ashley
McGuigan for help in the field. Alice Broadhead, Rene´e Marchin,
Matthew Hohmann, and William Hoffmann provided helpful comments
on the manuscript.
Author Contributions
Conceived and designed the experiments: JLS MGJ. Performed the
experiments: JLS MGJ. Analyzed the data: JLS MGJ. Contributed to the
writing of the manuscript: JLS MGJ.
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