The role of understory phenology and productivity in the carbon
dynamics of longleaf pine savannas
CHRISTINA L. STAUDHAMMER,
CHLOE L. JAVAHERI,
J. KEVIN HIERS,
LINDSAY R. BORING,
ROBERT J. MITCHELL,
AND GREGORY STARR
Department of Biological Sciences, University of Alabama, Tuscaloosa, Alabama 35487 USA
Tall Timbers Research Station, 13093 Henry Beadel Dr., Tallahassee, Florida 32312 USA
Joseph W. Jones Ecological Research Center, Newton, Georgia 39870 USA
Citation: Wiesner, S., C. L. Staudhammer, C. L. Javaheri, J. K. Hiers, L. R. Boring, R. J. Mitchell, and G. Starr. 2019. The
role of understory phenology and productivity in the carbon dynamics of longleaf pine savannas. Ecosphere 10(4):
Abstract. Savanna ecosystems contribute ~30% of global net primary production (NPP), but they vary
substantially in composition and function, speciﬁcally in the understory, which can result in complex
responses to environmental ﬂuctuations. We tested how understory phenology and its contribution to
ecosystem productivity within a longleaf pine ecosystem varied at two ends of a soil moisture gradient
(mesic and xeric). We used the Normalized Difference Vegetation Index (NDVI) of the understory and
ecosystem productivity estimates from eddy covariance systems to understand how variation in the under-
story affected overall ecosystem recovery from disturbances (drought and ﬁre). We found that the mesic
site recovered more rapidly from the disturbance of ﬁre, compared to the xeric site, indicated by a faster
increase in NDVI. During drought, understory NDVI at the xeric site decreased less compared to the mesic
site, suggesting adaptation to lower soil moisture conditions. Our results also show large variation within
savanna ecosystems in the contribution of the understory to ecosystem productivity and recovery, high-
lighting the critical need to further subcategorize global savanna ecosystems by their structural features, to
accurately predict their contribution to global estimates of NPP.
Key words: drought; ﬁre; Normalized Difference Vegetation Index; net ecosystem production; prescribed ﬁre; savanna
Received 4 September 2018; revised 20 February 2019; accepted 26 February 2019. Corresponding Editor: Dawn M.
Copyright: ©2019 The Authors. This is an open access article under the terms of the Creative Commons Attribution
License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Understory vegetation is thought to play a key
role in carbon dynamics of ecosystems across the
globe. Uncertainties exist, however, regarding
the total carbon found in this vegetation strata
(Johnson et al. 2017, Refsland and Fraterrigo
2017), and these uncertainties are expected to
increase as climatic extremes become more com-
mon and severe (IPCC 2014). These shifts in cli-
mate, particularly drought, will have a direct
effect on ecosystem structure (both understory
and overstory), function (phenology and physiol-
ogy), and ultimately their management strategies
(Rich et al. 2008, Becknell et al. 2015). Quantify-
ing phenological changes and understory carbon
dynamics is particularly difﬁcult using coarse
remote sensing techniques due to the canopy
variation in forests and/or uneven sensor
obstruction (Picotte and Robertson 2011). Fur-
thermore, critical variation of the understory
occurs at ﬁne (1–10 m
) spatial scales (Hiers et al.
2009, Starr et al. 2015). This is especially the case
for savanna and woodland ecosystems where
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canopies can be relatively open and less uniform,
and therefore harder to classify using coarse spa-
tial scales of satellite-derived remote sensing
products (Patenaude et al. 2004, Simard et al.
2011, Smith et al. 2014).
Understanding savanna structure and function
is critically important, as savannas cover ~15% of
the global land surface (Ma et al. 2013) and con-
tribute ~30% to global net primary production
(NPP, Field et al. 1998, Fei et al. 2017), thus repre-
senting a signiﬁcant portion of the global carbon
cycle (Bombelli et al. 2009). Nevertheless,
savanna ecosystems vary across the globe based
on their underlying geology and regional climates
(Bond et al. 2003, Vaughn et al. 2015). Differences
among and within savannas often result in com-
plex responses to environmental ﬂuctuations
en et al. 2016, Starr et al. 2016). For
example, savanna ecosystems were shown to
exhibit different responses to drought, even
within the same region (Starr et al. 2016). This
ﬁnding has been linked to variations in soil water-
holding capacity, which in turn has led to varia-
tions in plant functional types among sites
(Vaughn et al. 2015). Differences in plant func-
tional types can drive changes in phenological
patterns, as well as differential response to distur-
bances (Rich et al. 2008, Bernhardt-R€
et al. 2011, Wu et al. 2016). Thus, inclusion of site-
speciﬁc phenology is extremely important in
making accurate predictions regarding physio-
logical patterns and ecosystem carbon dynamics.
These patterns, however, are poorly represented
in global dynamic vegetation models and are a
source of systematic errors in regional to global
scale model predictions (Boke-Ol
en et al. 2016).
Complicating our understanding of ecosystem
carbon and energy dynamics is the fact that dis-
turbance events result in differing responses
between the understory and the overstory (Rich
et al. 2008). The understory in forests and wood-
lands can contribute roughly 30–50% to the
annual carbon ﬂuxes of an ecosystem (Powell
et al. 2008, Bracho et al. 2012). However, this
response varies across the landscape and may
change with increasing frequencies of the distur-
bance (Mitchell et al. 2014). A study on North
American savannas revealed that the understory
was more capable of rapidly utilizing newly
available resources following a prolonged
drought compared to the overstory (Rich et al.
2008). This rapid shift to resource availability off-
set the whole ecosystem decline in function and
accelerated recovery from the disturbance (Rich
et al. 2008). In contrast, Ma et al. (2013) showed
that increasing temporal variability in phenology
coincided with decreasing tree–grass ratios,
which suggest that higher woody fractions in the
understory promote higher stability and resili-
ence to future climate change. Collectively, these
studies highlight the inﬂuence of site-speciﬁcabi-
otic and biotic factors that drive savanna over-
story and understory phenological patterns and
ultimately the ecosystem’s carbon dynamics.
Savanna understory vegetation also plays a
key role in enabling the efﬁcient spread of sur-
face ﬁres through these ecosystems, which main-
tains the ecosystem’s structure and function
(Barlow et al. 2015). With a bare or patchy
understory, ﬁre would not effectively spread
across the ﬂoor and therefore enable the expan-
sion of woody shrubs (Mitchell et al. 2006), lead-
ing to a shift in the ecosystem structure (Peterson
and Reich 2007), and hence a shift in ecosystem
carbon dynamics. Changes in structure can also
precipitate declines in biodiversity (Walker and
Peet 1984) which further alter the carbon cycling
in savanna ecosystems (Mitchell et al. 1999, Kirk-
man et al. 2016a). However, the degree to which
ﬁres interact with understory regrowth, espe-
cially during drought, has yet to be fully under-
stood. How ﬁre alters the overall carbon ﬂuxes of
the ecosystem, as a function of understory
regrowth, varies substantially across different
ecosystems. A study conducted in a longleaf pine
ecosystem found that physiological activity and
hence productivity returned to pre-ﬁre levels
only 30–60 d post-ﬁre (Starr et al. 2015). A sepa-
rate study in a mixed longleaf slash pine forest in
north central Florida (USA) suggested that 70%
of understory N and C pools are consumed by
managed burns, but recover within three years
post-ﬁre (Lavoie et al. 2010). These studies, how-
ever, were short in nature—following a single
ﬁre cycle, showing the need for longer term
observations to cover greater environmental con-
ditions and multiple ﬁre cycles.
Longleaf pine savannas of the southeastern
United States are ideal for these studies since
their canopies are open and dominated by lon-
gleaf pine, Pinus palustris (Mill.), while their
understories host a remarkably high quantity of
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WIESNER ET AL.
species when compared to other temperate
ecosystems (Walker and Peet 1984, Kirkman
et al. 2004). Up to 50 species per m
found within the understory, mostly on poorly
drained soil (Walker and Peet 1984, Kirkman
et al. 2001), whereas drier and sandier soils often
have lower biodiversity in the understory
(Goebel et al. 2001, Kirkman et al. 2001). The rel-
ative species diversity in longleaf pine savannas
is often attributed to differences in nutrient
availabilities in the soil, as more mesic sites usu-
ally have higher proportions of clay in the soil,
which has been shown to drastically lower nutri-
ent availability (Metz 1952, Christensen 1977,
Quantifying understory phenology, as a func-
tion of differences in understory composition,
and its contribution to regional and global car-
bon budgets can be tedious and time-consuming
and may even be problematic (Johnson et al.
2017). However, the Normalized Difference
Vegetation Index (NDVI; Boke-Ol
en et al. 2016)
has been demonstrated to be advantageous in
determining the magnitude of ecosystem carbon
and energy ﬂuxes (Potter 1999), as well as in
quantifying understory phenology (Glenn et al.
2008). For example, NDVI has been used to
extract phenophases (greenup, maturity, senes-
cence, and dormancy; Zhang et al. 2003) and pre-
dict leaf phenological patterns (Xu et al. 2014) for
temperate deciduous trees. NDVI was also suc-
cessfully used to quantify phenology patterns at
FLUXNET sites; however, the accuracy
depended on the plant functional types present
at each site (Balzarolo et al. 2016). Other studies
have used NDVI estimates to quantify food
availability and nutritional quality for avian her-
bivores, showing that using handheld instru-
ments to measure NDVI had a higher accuracy
compared to satellite-derived measures (Hogrefe
et al. 2017).
The spatial resolution of NDVI measures is
critical for interpretation of ecological relevance.
Studies have found that utilizing temporal and/or
spatial resolutions that are too coarse lowers pre-
diction accuracy when studying interannual phe-
nological patterns or biomass productivity (Gatis
et al. 2017). The course nature of satellite-derived
NDVI measures in evergreen forests has been
shown to be a better measure of ecosystem struc-
ture and function, rather than gross ecosystem
productivity (GEP; Restrepo-Coupe et al. 2016).
These studies highlighted the usefulness of
NDVI measures and its limitations with respect
to coarse spatial scales. This underlines the need
for increased use of ground-based remote sens-
ing techniques, especially when site-speciﬁc char-
acteristics play an important role in the
productivity of the ecosystem of interest
(Hogrefe et al. 2017).
Using sub-canopy remote sensed products, the
overall objective of this study was to determine
the contribution of understory phenology to
ﬂuxes at the ends of a soil mois-
ture gradient with respect to prescribed ﬁre and
seasonal drought. We used monthly understory
NDVI measurements to quantify productivity at
two longleaf pine sites representing the ends of
this gradient (mesic and xeric). We hypothesized
that (1) the xeric site would recover more rapidly
from drought as it evolved under lower soil
moisture conditions; (2) ﬁre would lower under-
story NDVI at both sites, with the mesic site
understory recovering more rapidly post-ﬁre due
to higher soil water availability; and (3) under-
story NDVI would be associated with increased
ecosystem productivity at both sites, with the
xeric site exhibiting greater inﬂuence of the
understory on overall carbon ﬂuxes due to its
more open canopy.
MATERIALS AND METHODS
The study was conducted from August 2011
through to March 2016 in southwest Georgia,
USA (31.2201°N, 84.4792°W), within the South-
eastern Coastal Plain, at the Joseph W. Jones Eco-
logical Research Center (JWJERC; Fig. 1). The
area receives on average 1310 mm of rain annu-
ally and is climatically categorized as humid sub-
tropical (Christensen 1981, Goebel et al. 2001).
The long-term average monthly air temperatures
range from 9.6°C to 27.6°C in January and July,
Locations for this study were established in
two sites that represent the xeric and mesic ends
of an edaphic gradient in longleaf pine ecosys-
tems at the JWJERC and are located ~5.0 km
from one another (Fig. 1; Kirkman et al. 2001).
The xeric site was characterized by deep sandy
soils classiﬁed as typic quartzipsamments
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WIESNER ET AL.
without an argillic horizon in the upper 300 cm
of soil, with a water-holding capacity of approxi-
mately 18 cm of water per meter of soil, because
of the high porosity and underground drainage
in the soil (Goebel et al. 2001, Kirkman et al.
2001). The mesic site had a soil composition that
consisted of sandy loam that rested on top of
either clay or sandy clay loam soils. The mesic
Fig. 1. Land cover map of the Joseph W. Jones Ecological Research Center in southeast Georgia, USA, showing
the (A) mesic and (B) xeric sites. Blue circles show eddy covariance tower locations, and orange circles are the
tower footprints at the three sites.
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WIESNER ET AL.
site soils were not well drained and characterized
as arenic paleudults. The argillic horizon of these
soils was within ~95 cm, and the water-holding
capacity was 40 cm per m of soil in the upper
300 cm (Goebel et al. 2001, Kirkman et al. 2001).
The relatively small discrepancies between the
site characteristics contributed to a large distinc-
tion between the sites’species composition and
vegetation structure (Kirkman et al. 2001).
Both sites were comprised of an open longleaf
pine canopy in the overstory and wiregrass (Aris-
tida beyrichana Trin.) in the understory, while the
composition of secondary species varied by site
(Kirkman et al. 2001). Both ecosystems were
woodland systems with basal areas of 11.1 and
/ha at the xeric and mesic sites, respec-
tively, of which ~18% were oak trees at the xeric
site versus 6% at the mesic site. Due to differ-
ences in soil drainage, understory species rich-
ness was signiﬁcantly higher at the mesic site
compared to the xeric site (Kirkman et al. 2016a).
The understory of the xeric site, however, had a
higher density of native hardwoods relative to
the mesic site, with the scrub oak species Quercus
laevis Walt. and Quercus margaretta Ashe found
most prevalently. The mesic site had a lower con-
centration of oaks present, and instead, a higher
population of common persimmon Diospyros vir-
giniana L. found most frequently in the under-
story (Goebel et al. 2001). The overstory leaf area
index (LAI) for the mesic site ranged from 0.65 to
, while at the xeric site, it ranged from
0.22 to 0.65 m
(Addington et al. 2006,
Wright et al. 2013). Both the mesic and xeric sites
have been thoroughly described in previously
published works by Mitchell et al. (1999), Kirk-
man et al. (2001), Ford et al. (2008), and Starr
et al. (2015).
Four productivity plots, 50 950 m in size,
were established prior to this study at each site.
These plots were located within the ﬂux footprint
of each site’s eddy covariance tower (~500 m
radius from the tower). Understory composition
at both sites was estimated annually during each
fall within the four plots, with the exception of
2014 and 2016, due to a change in the sampling
protocol from annual measurements to 2-yr mea-
surement cycles in 2013. The understory biomass
was estimated using 0.75-m
clip plots. A plot
frame was randomly tossed from each of seven
litter trap positions, which had been previously
established within the plots at the two sites,
resulting in a total of 28 replicates at each site.
Where the frames touched the forest ﬂoor, all live
and dead vegetation smaller than 1 meter in
height was clipped and brought to the laboratory
for analyses. The vegetation was then classiﬁed
by growth form into forbs, ferns, legumes, other
grasses, and woody plants. The biomass from
the plots was then dried to a constant weight.
The Palmer Drought Severity Index (PDSI) for
the study period was obtained from the National
Oceanic Atmospheric Administration (NOAA)
and the National Centers for Environmental
Information (NCEI), Ashville, North Carolina,
USA (National Oceanic and Atmospheric
Administration, Department of Commerce n.d.).
The index describes severity of a drought on a
scale from 5to+5, where more negative num-
bers indicate more severe drought. The index is
computed using air temperature, rainfall, and
soil moisture measurements at climate stations
around the globe (Palmer 1965, Dai et al. 2004).
The two sites were burned frequently prior to
the study, averaging a two-year ﬁre return inter-
val since 1994 with the last burn prior to the
study occurring in 2009. During our study, the
sites experienced 3 burns, during springs of 2011,
2013, and 2015. Strip head ﬁres were set every
30–50 m (depending on the local ﬁre conditions
at the time of the burn) starting downwind of the
management unit and moving upwind (Hiers
et al. 2009). No damage to overstory trees was
recorded following the prescribed ﬁres, and as
ﬁres typical to this surface ﬁre regime are low
intensity (O’Brien et al. 2016), ﬂame heights are
typically below 2 m, thus unable to reach over-
story crowns which are on average 23 m above
the forest ﬂoor (Robertson and Ostertag 2007,
Varner et al. 2007, Whelan et al. 2013). While the
two study sites had prescribed ﬁres on a two-
year cycle, there was no control site that was
absent of prescribed ﬁres, due to rapid ecosystem
movement toward an alternative stable state
when deprived of prescribed ﬁres (O’Brien et al.
2010). If prescribed ﬁre is withheld for as little as
4 yr, the ecosystem structure, composition, and
function change (Kirkman et al. 2013).
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WIESNER ET AL.
In addition to data collected describing under-
story vegetation composition, we sampled
aboveground litter and understory biomass
before and after the ﬁres, using methods
described in Ottmar et al. (2007). The number of
clip plots sampled at the two sites varied from 10
to 20, such that a standard error of the mean of
~15% was achieved (Whelan et al. 2013). In 2011,
2013, and 2015, we collected aboveground bio-
mass within two weeks pre- and post-ﬁre using
clip plots at the mesic and xeric
sites (Table 1). Clip plots at both sites were
located along a transect and sampled every 25 m
starting at the base of each ﬂux tower and
extending within the ﬂux footprint (~500 m) in
the direction of the prevailing wind (Whelan
et al. 2013). Harvested clip plot litter and bio-
mass were dried to a constant weight and mass,
and fuel consumption was calculated as the dif-
ference of pre-burn and post-burn dry weight
(Whelan et al. 2013).
Understory NDVI was measured monthly
using a Tetracam ADC camera attached to a tri-
pod, which was placed consistently at 1.60 m
above each subplot for each measurement.
Because the xeric site was spatially more com-
plex than the mesic site, four plots were estab-
lished within the footprint at the xeric site,
whereas the mesic site was sufﬁciently repre-
sented by only three plots. In both sites, four 1-
subplots were located 10 m from the center of
each plot, one in each of the four cardinal direc-
tions (north, east, south, and west). Because the
camera ﬁeld of view could not span the entire
, four pictures were taken in each of the four
subplot corners, which were processed electroni-
cally and averaged during the post-processing
procedure. Before each subplot measurement,
the camera was calibrated using a white Teﬂon
calibration chip, to account for changes in reﬂec-
tive values due to weather conditions. Post-pro-
cessing was performed using the Pixelwrench II
software (Tetracam, Chatsworth, California,
USA), which calculates understory NDVI from
the red (Red) and near-infrared (NIR) reﬂectance
values of each image as
NDVI ¼ðNIR RedÞ=ðNIR þRedÞ:
Ecosystem flux measurements
Eddy covariance towers, positioned at each
site, measured net ecosystem exchange of CO
(NEE), as well as meteorological variables such
as rainfall, air temperature (T
), and photosyn-
thetic active radiation (PAR) above the canopy
(Whelan et al. 2013). In addition, soil moisture
(SWC) and soil temperature, as well as ground
heat ﬂux, were measured in a soil array adjacent
to the tower. NEE was measured via an
open-path eddy covariance method through a
simpliﬁcation of the continuity equation and
converted from lmolm
to g C/m
30 min. Missing half-hourly data were gap-ﬁlled
using separate functions for NEE during day-
time and nighttime. When photosynthetically
active radiation (PAR) was ≥10 lmolm
daytime NEE data were gap-ﬁlled using a
Michaelis–Menten approach, and when PAR was
, nighttime NEE data were
gap-ﬁlled using a modiﬁcation of the Lloyd and
Taylor (1994) approach, both on a monthly basis.
Where too few observations were available to
produce stable and biologically reasonable
parameter estimates, annual equations were used
to gap-ﬁll data by site. Gross ecosystem exchange
(GEE) was calculated from the difference of
NEE and ecosystem respiration (R
) as GEE =
. NEE, GEE, and R
summed up to monthly estimates. Daytime R
was estimated using nighttime gap-ﬁlling equa-
tion to partition NEE. A detailed explanation of
the equipment and ﬂux processing method can be
found in Starr et al. (2016) and Whelan et al.
(2013). Finally, we converted NEE and GEE to net
ecosystem productivity (NEP) and gross ecosys-
tem productivity (GEP), where positive values
Table 1. Understory biomass and fuel consumption
pre- and post-prescribed burns in 2011, 2013, and
2015 at the mesic and xeric sites.
2011 Mesic 1052.2 334.9 717.3
Xeric 780.5 425.7 354.8
2013 Mesic 957.7 523.5 434.2
Xeric 937.0 917.6 19.4
2015 Mesic 1643.1 440.8 1202.3
Xeric 1808.1 668.0 1140.1
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WIESNER ET AL.
indicate C uptake by the ecosystem and negative
values C release to the atmosphere.
Prior to the analysis of NDVI and ecosystem
ﬂuxes, we formulated simple linear mixed models
to quantify differences in SWC, T
between the two sites, using site, year, ﬁre-cycle
time (FCT), and their interactions as independent
variables. The factor FCT was included to describe
the amount of time that had passed since pre-
scribed burning. Following Whelan et al. (2013),
and third 28 d following ﬁre, respectively. These
categories comprised spring and the beginning of
summer. FCT 4 and 5 represented the next 140
and further 225 d following FCT 3, encompassing
late summer and fall. Pre-ﬁre (pf) indicated the
time before the next ﬁre (~10 months). We used
the lme function from the package nlme in R ver-
sion 3.4.3 (R Core Team 2013), including a ran-
dom effect to account for monthly repeated
measurements and the subplot design, as well as
an autocorrelations structure to account for the
correlation between adjacent time points.
We then estimated linear mixed models for
each of the response variables: monthly mean
NDVI and monthly sums of NEP, GEP, and R
For the NDVI model, we included ﬁxed effects
for site, PDSI, FCT, mean monthly PAR, and
mean SWC, as well as the interactions of site
with PDSI and FCT, FCT and PAR, and FCT.
The NEP, GEP, and R
models included ﬁxed
effects for year, month, FCT, site, PDSI, and the
interactions of site with FCT, PDSI, and NDVI,
as well as the interaction between FCT and
NDVI. Mean PAR and SWC were also included
as ﬁxed effects in these models. We also tested
the models using T
instead of PAR, which
resulted in similar trends of the response vari-
ables, as well as similar AIC (Akaike informa-
tion criterion) values. We could not include both
variables as their high correlation (>0.8) would
have led to multicollinearity in the independent
variables. We chose PAR for our ﬁnal models to
quantify changes in NDVI and ecosystem ﬂuxes
in response to changes in incoming energy. For
each response variable, we used a modiﬁed
backward selection criterion to choose the best,
most parsimonious model. Non-signiﬁcant
(P>0.05) variables were eliminated, as long as
it resulted in a lower (better) AIC value. Where
interactions were signiﬁcant, the underlying
simple effects were retained in the model
regardless of signiﬁcance. We examined the nat-
ure of signiﬁcant differences of all interactions
using the lsmeans function in R (Lenth 2016),
whereby marginal means are computed holding
all other independent variables at their average
Annual rainfall was ~800 mm during 2011 and
2012 (Fig. 2A), lowering the PDSI (Fig. 2A) to
<4. Annual rainfall sums increased to
~1500 mm during 2013, which lead to an
increase in PDSI to >0, followed by another
decrease during 2015 (Fig. 2A). Soil moisture
was signiﬁcantly lower at the xeric site compared
to the mesic site for all years and levels of FCT.
Additionally, SWC was signiﬁcantly lower at
both sites during the drought (Fig. 2B), while
SWC returned to pre-drought levels at the end of
2012 as rainfall recovered (Fig. 2A). Mean
monthly PAR decreased during the wetter years,
but this difference was not signiﬁcant (Fig. 2C).
Average PAR was signiﬁcantly higher at the xeric
site (by ~30–60 lmolm
) compared to the
mesic site for all years except 2015, when
PAR was signiﬁcantly higher at the mesic site (by
). Furthermore, PAR was signiﬁ-
cantly higher at the xeric site compared to the
mesic site for all levels of FCT, except for pre-ﬁre.
Values of T
were higher (>30°C) during 2011
and then decreased below 30°C during summer
of the following years (Fig. 2D). Understory
NDVI during the growing season in 2011 was
lower at both sites with gradual increases in sub-
sequent years (Fig. 3A) and further increases in
the summer months of 2014 and 2015. During
winter months, NEP and GEP were lower at the
xeric site compared to the mesic site (Fig. 2B, C).
decreased slightly at both sites during 2015,
but GEP was only slightly lower during the win-
ter months of that year (Fig. 3D).
Understory NDVI phenology under drought and
Forbs, grasses, and wiregrass comprised a
greater proportion of the understory at the mesic
site, speciﬁcally outside of drought years,
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WIESNER ET AL.
whereas woody understory species were more
abundant at the xeric site, especially during the
drought (Fig. 4).
Model results indicated that NDVI varied signiﬁ-
cantly by site, but its effect depended on SWC, PAR,
PDSI, and time since ﬁre (FCT). Pre-ﬁre (pf) under-
story NDVI was slightly higher at the mesic site
(~0.48), compared to the xeric site (~0.43, Table 2,
Fig. 5). Following the prescribed ﬁre, NDVI at the
xeric site decreased during FCT 1 (~0.26). How-
ever, no signiﬁcant change was observed from
FCT 1 through FCT 3 (28–54 d post-ﬁre, Fig. 5A).
NDVI at the mesic site also decreased to ~0.41–
0.43 during FCT 1 and FCT 2, followed by an
increase in FCT 3 to ~0.47 and a further increase
during FCT 4 to 0.66, which was signiﬁcantly dif-
ferent from NDVI during FCT 2 (Fig. 5). During
FCT 5, NDVI at the mesic site signiﬁcantly
decreased to 0.53. NDVI at the xeric site signiﬁ-
cantly increased during FCT 5 (~0.66), followed
by a signiﬁcant decrease in FCT 5 to ~0.42.
NDVI signiﬁcantly decreased with an increase
in PDSI at both sites, with less of a decrease at the
xeric site (Fig. 5B). In addition, the xeric site had
signiﬁcantly lower NDVI for all levels of PDSI.
NDVI signiﬁcantly decreased for the levels of
FCT 5 and pre-ﬁre but showed no signiﬁcant
change for FCT 1–3, when average PAR increased
to 500 lmolm
. For the interaction of FCT 4
and PAR, NDVI signiﬁcantly decreased by ~0.5
when PAR increased, but exceeded 1, when PAR
was below 100 lmolm
(Fig. 5). NDVI
decreased by 0.3 with increases in SWC (from
17% to 24%), but these effects were not signiﬁ-
cantly different by site.
Understory NDVI effects on NEP
Net ecosystem productivity was signiﬁcantly
different by site and was driven by NDVI, FCT,
PAR, time since ﬁre, and PDSI (Table 3). The
mesic site NEP signiﬁcantly decreased with
increases in NDVI compared to the xeric site
Fig. 2. Monthly (A) summed rainfall (mm) and Palmer Drought Severity Index (PDSI), that is, gray line with its
corresponding y-axis on the right-hand side of panel (A), mean (B) soil water content (SWC; %), (C) photosynthetic
active radiation (PAR; lmols
), and (D) air temperature (T
;°C) from August 2011 through March 2016.
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WIESNER ET AL.
Fig. 3. Monthly (A) mean values of the Normalized Difference Vegetation Index (NDVI) and summed (B) net
ecosystem productivity (NEP), (C) gross ecosystem productivity (GEP), and (D) ecosystem respiration (R
from August 2011 through March 2016. Arrows indicate the time of prescribed ﬁre at the mesic and xeric
Fig 4. Annual understory live biomass by plant type at the mesic and xeric sites from 2011 to 2015.
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WIESNER ET AL.
(Fig. 6A, Table 3). Monthly NEP was signiﬁ-
cantly lower at the xeric compared to the mesic
site pre-ﬁre but increased (greater carbon uptake)
following the ﬁre (Fig. 6B). NEP at the mesic site
signiﬁcantly increased following the ﬁres during
FCT 1 and 2 (up to 40 g C/m
per month). Fol-
lowing FCT 2, NEP decreased at the mesic site to
values similar to those of the xeric site (20–10 g
per month). Both sites were weaker carbon
sinks when drought increased (Fig. 6C). NEP sig-
niﬁcantly increased when PDSI moved toward
zero, with the mesic site being a greater carbon
sink than the xeric site.
As NDVI increased, so did NEP during FCT 2
and FCT 3, which was statistically signiﬁcant.
During FCT 4, the opposite pattern was
observed, where higher NDVI resulted in lower
NEP (Fig. 6D). Photosynthetically active radia-
tion signiﬁcantly increased the carbon sink
strength at both sites, with no signiﬁcant differ-
ence between the mesic and xeric sites (Fig. 7A).
Understory NDVI effects on GEP
Similar to that of NEP, there was a signiﬁcant
difference in GEP by site which was correlated
with NDVI, FCT, and PDSI (Table 3). There was
also a signiﬁcant effect of NDVI with FCT and a
simple effect of PAR, which was not signiﬁcantly
different by site (Table 3). When NDVI was
below 0.5, monthly GEP at the mesic site was sig-
niﬁcantly higher (160 g C/m
per month) than
the xeric site (145 g C/m
per month). When
NDVI (>0.75) increased, GEP decreased slightly
at the mesic site, but increased at the xeric site
such that it had higher productivity than the
mesic site (Fig. 8A).
Preceding the prescribed burn GEP was not
signiﬁcantly different at the xeric site, and this
persisted through FCT 2, although NDVI was
lower (Fig. 8B). During FCT 3, GEP increased
from 140 to 160 g C/m
per month at the xeric
site, which then remained at that rate for FCT 4
and FCT 5. The mesic site experienced a slight
decrease in GEP during FCT 1, followed by an
increase to approximately 170 g C/m
month and a steep decrease in GEP during
FCT 3 and FCT 4 (140 g C/m
Then, in FCT 5, the mesic site increased its pro-
ductivity to roughly 155 g C/m
Higher NDVI signiﬁcantly increased GEP
Table 2. Type 3 tests of ﬁxed effects for the model of
the Normalized Difference Vegetation Index
value df P-value
(Intercept) 43.59 1 <0.0001
PDSI 1.042 1 0.307
Site 47.17 1 <0.0001
FCT 18.58 5 0.002
SWC 68.57 1 <0.0001
PAR 19.84 1 <0.0001
Site:FCT 36.06 5 <0.0001
Site:SWC 115.98 1 <0.0001
PDSI:Site 5.42 1 0.0198
Notes: df, degrees of freedom (numerator). P-value
corresponds to chi-squared statistic with df.
Fig. 5. Least square mean values of Normalized Difference Vegetation Index (NDVI) by site and (A) ﬁre-cycle
time (FCT) and (B) Palmer Drought Severity Index (PDSI; 5 to 5), and by (C) FCT and photosynthetic active
radiation (PAR). Error bars indicate 1 standard error (SEM). FCT 1, 2, and 3 correspond to the ﬁrst, second, and
third 28 d following ﬁre. FCT 4 and 5 represented the next 140 and further 225 d following FCT 3. Pre-ﬁre (pf)
indicated the time before the next ﬁre (~10 months).
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WIESNER ET AL.
during pre-ﬁre, and FCT 2 and 3, but decreased
its magnitude during FCT 4 across both sites
(Fig. 8D). Interestingly, GEP increased with
decreasing PAR and PDSI at both sites (Figs. 7B
Understory NDVI effects on R
Model results indicated that R
cantly different by site and also depended on
PDSI, FCT, and NDVI. Increases in understory
NDVI increased R
at the mesic site, but only
slightly changed the magnitude of R
xeric site. These changes in R
, however, were
not signiﬁcant across NDVI levels (Fig. 9A). R
was signiﬁcantly lower at the mesic site for all
levels of NDVI, compared to the xeric site.
Fire affected R
differently by site (Fig. 9B).
signiﬁcantly decreased at the mesic site,
following the ﬁre during FCT 1 (122 g C/m
month), slightly increased during FCT 2 (127 g
per month) and decreased further during
FCT 3 and 4 (~120 g C/m
per month). R
xeric site decreased only slightly during FCT 1–2,
followed by an increase to ~145 g C/m
month during FCT 3 and 4. The mesic site
increased its R
during FCT 5, back to ~135 g
per month, whereas the xeric site decreased
to ~140 C/m
per month. Negative values of
PDSI increased R
at both sites. However, this
was more pronounced at the xeric site (Fig. 9C).
For levels of PDSI >3, both sites had monthly
rates of ~120 g C/m
per month, with signiﬁ-
cantly higher rates at the xeric site throughout
this study. Increases in PAR signiﬁcantly
decreased the magnitude of R
, with no signiﬁ-
cant difference by site (Fig. 7C).
Our study demonstrates that understory vege-
tation in longleaf pine ecosystems plays a com-
plex role in patterns of carbon uptake and
release. The understory phenology and composi-
tion contribute signiﬁcantly to the overall pro-
ductivity of this ecosystem. More importantly,
our results reveal that site characteristics play a
critical role in how understories mediate ecosys-
tem recovery from drought and prescribed ﬁre.
We show that changes in understory biomass
(higher NDVI) signiﬁcantly affected GEP during
recovery from ﬁre. We found increased photo-
synthetic capacity between two and three
months after the ﬁres when understory biomass
was high. However, this relationship shifted after
four months, resulting in a decrease in photosyn-
thetic activity when NDVI was greater (Jurik
1986, Hikosaka 2005). This altered response high-
lights the need to incorporate understory phenol-
ogy when studying ecosystem recovery and
resilience in open forest stands. It further demon-
strates that the capacity of ecosystems to seques-
ter carbon depends on changes in understory
biomass over the course of the year (Chen et al.
For example, minor decreases in GEP at the
mesic site occurred with increasing NDVI indi-
cated that the understory contributed less to GEP
and that the overstory was the primary driver of
ecosystem productivity at the site (Yang et al.
Table 3. Type 3 tests of ﬁxed effects for the models of
net ecosystem productivity (NEP), gross ecosystem
productivity (GEP), and ecosystem respiration
Model Effect v
value df P(>v
NEP NDVI >0.01 1 0.965
FCT 61.91 5 <0.0001
PDSI 2.28 1 0.131
PAR 97.80 1 <0.0001
Site 1229.33 1 <0.0001
NDVI:Site 102.33 1 <0.0001
PDSI:Site 22.98 1 <0.0001
NDVI:FCT 13.21 5 0.022
FCT:Site 311.50 5 <0.0001
GEP NDVI 2.69 1 0.101
FCT 57.93 5 <0.0001
PDSI 0.49 1 0.482
PAR 15.08 1 <0.0001
Site 705.64 1 <0.0001
NDVI:Site 53.22 1 <0.0001
PDSI:Site 3.87 1 0.049
NDVI:FCT 13.16 5 0.022
FCT:Site 552.07 5 <0.0001
NDVI 9.37 1 0.002
FCT 13.50 5 0.019
PDSI 1.59 1 0.208
SWC 2.49 1 0.115
PAR 447.69 1 <0.0001
Site 70.56 1 <0.0001
NDVI:Site 9.80 1 0.002
PDSI:Site 122.72 1 <0.0001
FCT:Site 466.00 5 <0.0001
Notes: df, degrees of freedom (numerator). P-value
corresponds to chi-squared statistic with df.
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WIESNER ET AL.
2017). This resulted in lower photosynthetic
capacity at the site when NDVI was high, com-
pared to the xeric site, as it is dominated by lon-
gleaf pine and grass species in the understory
(~30%; Wiesner et al. 2018). Furthermore,
biomass and leaf area were higher at the mesic
site, compared to the xeric site, suggesting less
solar radiation was reaching the understory,
which in turn could decrease productivity rela-
tive to the xeric site (Starr et al. 2016). Even
Fig. 6. Least square mean values of net ecosystem productivity (NEP) by site and (A) Normalized Difference
Vegetation Index (NDVI), (B) ﬁre-cycle time (FCT), and (C) the Palmer Drought Severity Index (PDSI), and by
(D) FCT and NDVI. Error bars indicate 1 standard error (SEM). FCT 1, 2, and 3 correspond to the ﬁrst, second,
and third 28 d following ﬁre. FCT 4 and 5 represented the next 140 and a further 225 d following FCT 3. Pre-ﬁre
(pf) indicated the time before the next ﬁre (~10 months).
Fig. 7. Least square mean values of (A) net ecosystem productivity (NEP), (B) gross ecosystem productivity
(GEP), and (C) ecosystem respiration (R
) across levels of photosynthetic active radiation (PAR). Error bars indi-
cate 1 standard error (SEM).
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WIESNER ET AL.
though basal area, leaf area, and understory
NDVI were lower at the xeric site, R
higher with lower NDVI. These ﬁndings were
likely a result of greater maintenance respiration
of the oak dominated overstory during dor-
mancy (Amthor 1984, Wu et al. 2014). In addi-
tion, the understory at the xeric site had a
proportionally higher contribution to the ﬂux of
Fig. 8. Least square mean values of gross ecosystem productivity (GEP) by site and (A) the Normalized Vege-
tation Difference Index (NDVI), (B) ﬁre-cycle time (FCT), and (C) the Palmer Drought Severity Index (PDSI), and
by (D) NDVI and FCT. Error bars indicate 1 standard error (SEM). FCT 1, 2, and 3 correspond to the ﬁrst,
second, and third 28 d following ﬁre. FCT 4 and 5 represented the next 140 and further 225 d following FCT 3.
Pre-ﬁre (pf) indicated the time before the next ﬁre (~10 months).
Fig. 9. Least square mean values of R
by site and (A) the Normalized Difference Vegetation Index (NDVI),
(B) ﬁre-cycle time (FCT), and (C) the Palmer Drought Severity Index (PDSI). Error bars indicate 1 standard error
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WIESNER ET AL.
GEP, compared to the mesic site. This effect was
a result of higher abundance of woody species in
the understory and therefore higher photosyn-
thetic activity during peak NDVI, as broadleaved
shrubs and trees are known to have higher pho-
tosynthetic capacity compared to grasses and
coniferous trees (Weaver and Mogensen 1919,
Klein et al. 2013, Renninger et al. 2015).
We show that longleaf pine savannas are resili-
ent to the disturbance of ﬁre and drought, as a
result of their ability to rapidly mobilize non-
structural carbohydrates when photosynthate
supply is low, in agreement with a previous
study conducted at our sites (Aubrey and Teskey
2018). However, we found that the magnitude
and timescale of recovery was site-dependent.
The mesic site recovered more rapidly from the
disturbance of ﬁre, possibly as a result of a
higher species diversity in the understory (Kirk-
man et al. 2016b), which increases the potential
of certain understory species to rescue ecosystem
function (Elmqvist et al. 2003, Starr et al. 2015,
Wiesner et al. 2018). Understory NDVI and NEP
at the mesic site increased substantially more
during the ﬁrst three months following the ﬁre,
indicating rapid plant regrowth in the under-
story, potentially as a result of more readily avail-
able nutrients following the ﬁre (Lavoie et al.
2010). This is supported by a previous study con-
ducted at these sites, which found increased soil
respiration primarily at the mesic site for two
months after prescribed ﬁre. Our ﬁndings and
the ﬁndings from Wiesner et al. (2018) suggest
that more rapid understory plant biomass
regrowth at the mesic site increased respiration
rates, as a result of higher maintenance and
growth respiration. The grass dominated under-
story at the site also likely accelerated its recov-
ery time, as grasses make use of stored and
available resources more rapidly compared to
woody species (Brewer 2011). Furthermore,
higher soil moisture conditions at the site
enabled faster resource acquisition (White et al.
2016), which enhanced plant biomass regrowth
in contrast to the xeric site.
On the contrary, lower understory NDVI at the
xeric site following the ﬁre was likely a function
of lower fuel consumption compared to the
mesic site. Due to higher heterogeneity of the
understory vegetation on xeric sites, ﬁre did not
spread as uniformly (Duncan et al. 2015). This
would also contribute to smaller magnitude in
biomass regrowth following the ﬁres (Pinno and
Errington 2016), as reﬂected in the ecosystem
ﬂuxes compared to the mesic site. Even though
average N mineralization levels in the upper
soils were found to be higher at xeric sites (Bor-
ing et al. 2004), the heterogeneity in ﬁre effects
may have resulted in lower nutrient availability
within the upper soil layers post-ﬁre, compared
to the mesic site. Furthermore, similar N mineral-
ization rates at mesic and xeric sites below the
upper soil surface (<15 cm), as well as higher
SWC and higher root biomass at the mesic site
(Hendricks et al. 2006), would enable greater
nutrient availability and uptake (Lavoie et al.
2010). Moreover, sandy soils at the xeric site can
promote leaching of nutrients (Nguyen and
Marschner 2013), thereby decreasing nutrient
availability and thus plant regrowth.
However, the xeric site experienced a substan-
tial increase in NDVI, GEP, and R
following the prescribed burns. High R
GEP at the xeric site were indicative of the sea-
sonal increase in greenness and therefore meta-
bolic activity of deciduous oaks (Jurik 1986,
Hikosaka 2005, Powell et al. 2005), thereby
increasing growth respiration, as more recent
photosynthates were invested into bud and leaf
expansion (Keel and Sch€
adel 2010, Alla et al.
2013, Kuster et al. 2014, Herrmann et al. 2015).
In support of this notion, we found a decrease in
NEP for increasing NDVI during that time, sug-
gesting that more plant biomass in the under-
story increased respiration. In contrast, three
months following the burn, R
was lower at the
mesic site, but GEP continued to decrease for
FCT 4, which also resulted in lower carbon sink
capacity at the site. A similar response for the
mesic and xeric sites was found in Whelan et al.
(2013), who showed that the base respiration rate
decreased at the mesic site but increased at the
xeric site following the ﬁres. Another explanation
for lower metabolic activity at the mesic site dur-
ing FCT 4 and 5 was that average T
(>20°C) compared to T
for FCT 1–3(<20°C, evi-
dent from Fig. 2D), which would cause stomata
to close to conserve water (Gonzalez-Benecke
et al. 2011, Samuelson et al. 2012). For example,
longleaf pine trees were shown to decrease their
growth rates in response to warmer summer
temperatures (Foster and Brooks 2001), whereas
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WIESNER ET AL.
oak species are more resistant to higher T
anisohydric response; Roman et al. 2015).
Understory species at the xeric site were
shown to be less drought resilient compared to
those of its overstory. Even though the xeric site
is chronically exposed to lower soil moisture con-
ditions, we found that understory NDVI was sig-
niﬁcantly lower for all levels of PDSI compared
to the mesic site, showing that understory spe-
cies were not able to thrive at the level of that of
the mesic site under drought conditions. How-
ever, the magnitude of NDVI change (i.e., slope
of the regression) was lower at the xeric site
when severity of drought increased, indicating
that plant functional types at the site could buffer
drought conditions more effectively (Coble et al.
2017, Granda et al. 2018), such that understory
NDVI decreased by half as much as at the mesic
site. In addition, overall ecosystem productivity
at xeric sites was shown to recover more rapidly
from drought (Starr et al. 2016), compared to
more mesic sites, which was the result of
drought-resistant plant species in the over- and
understory (Wright et al. 2013). Oak components
have been shown to increase climate resilience
on xeric sites by facilitating longleaf pine regen-
eration (Loudermilk et al. 2016). We also showed
that differences in site productivity during
drought were mainly governed by differences in
photosynthetic activity, such that the xeric site
had similar levels of R
over the range of PDSI
but could not maintain similar levels of GEP,
compared to the mesic site.
In this study, the variation in phenology of the
understory vegetation played an important role
in the ecosystem’s response to disturbance. The
effects of prescribed ﬁre on NEP and post-ﬁre
recovery were mediated not only by site type but
also by interactions with variation in climate
(PDSI). The ability to sustain relatively high pho-
tosynthetic capacity (and respiration) during
drought at both sites has profound consequences
in relation to future changes in climate, if
droughts become more severe and frequent
(IPCC 2014). However, prolonged drought could
change the system from a carbon sink to a
source, as R
would increase over GEP, which
may lead to carbon starvation or hydraulic fail-
ure, depending on the severity of the event
(McDowell 2011, Zeppel et al. 2011, Klein 2015).
Furthermore, severe drought could cause a shift
in ecosystem structure, as a consequence of the
inability to manage these systems with pre-
scribed ﬁre, as drier conditions limit prescription
options for managers (Mitchell et al. 2014,
Chiodi et al. 2018).
Future climate scenarios for the Southeastern
Coastal Plain include more frequent extreme
weather events, such as hurricanes and severe
droughts, as well as differences in the amount
and timing of precipitation (IPCC 2014). Longleaf
pine ecosystems have been hypothesized to exhi-
bit higher resistance to these projected changes,
leading to renewed efforts for their restoration.
The success of these efforts will bring to the fore-
front the importance of accurate and unbiased
estimates of their NEP.
Our results demonstrate large differences
within savanna ecosystems in the contribution of
the understory to ecosystem productivity and
recovery, highlighting the critical need to evalu-
ate how variation in savanna structure affects
their contribution to global estimates of NPP.
Furthermore, the inclusion of site-speciﬁc phe-
nology would improve predictions regarding
physiological patterns and ecosystem carbon
dynamics, as represented in global dynamic veg-
etation models (Boke-Ol
en et al. 2016). Further
studies are needed to quantify these differences
to fully understand how multiple disturbances
interact over a range of structural variations in
savanna ecosystems across the globe.
Understory phenology and ﬁre are critical
drivers of productivity in many ecosystems
globally. We demonstrated that understory con-
tribution to ecosystem ﬂuxes is not uniform
across environmental gradients within a savanna
ecosystem, which affected ecosystem recovery
times and overall productivity at the sites. As
wildﬁre activities increase under changing
climate (Westerling et al. 2006) and ecosystem
management efforts increasingly focus on savanna
ecosystems (Brudvig 2011, Noss et al. 2015),
understanding climate and ﬁre controls on under-
story carbon assimilation across edaphic variation
will be critical for understanding ecosystem
For the longleaf pine savannas in this study,
xeric sites characterized by lower overstory
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WIESNER ET AL.
density were shown to have higher contributions
of the understory to overall ecosystem ﬂuxes,
which increased their carbon sink capacity when
understory NDVI was high. Native hardwood
components to the understory of xeric sites
exerted strong inﬂuence of phenological patterns
observed in this study. More mesic and more pro-
ductive sites experienced lower variability in
ecosystem ﬂuxes, as a result of the overstory dom-
inating ecosystem ﬂuxes, due to high basal and
Site recovery from ﬁre disturbance was context
speciﬁc to interannual rainfall. For example,
understories at more mesic sites recovered more
rapidly from prescribed ﬁres, which increased
their carbon sink potential. In contrast, xeric sites
showed little changes in NDVI and therefore
NEP, GEP, and R
following the ﬁres, which
resulted in little change in their sink capacity. In
contrast, xeric site understories were less affected
by drought, but did not improve overall ecosys-
tem recovery from the disturbance.
Savanna ecosystems do not exhibit uniform
ecosystem productivity and recovery from dis-
turbance as a result of variations in structure
from the underlying geology, which should be
incorporated in global classiﬁcations of savanna
porating site variations within savanna ecosystems
to accurately predict ecosystem function and recov-
ery from disturbances. Our results demonstrate
the need for more ﬁne-scale studies, especially in
ecosystems with large structural variations, to
accurately predict global carbon ﬂuxes.
The authors thank the Forest Ecology Laboratory’s
personnel, with special thanks to Tanner Warren,
Andres Baron-Lopez, and Scott Taylor, for data collec-
tion and provision during the study at the Joseph W.
Jones Ecological Research Center. CS and GS acknowl-
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tion (DEB EF-1241881 and EF-1702996).
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