Buried hurricane legacies: increased nutrient limitation and

decreased root biomass in coastal wetlands

AMANDA L. KUHN ,1 JOHN S. KOMINOSKI ,1, ANNA R. ARMITAGE ,2 SEAN P. CHARLES,1
STEVEN C. PENNINGS ,3 CAROLYN A. WEAVER ,4 AND TOM R. MADDOX5
1
Department of Biological Sciences, Florida International University, Miami, Florida 33199 USA
2
Department of Marine Biology, Texas A&M University at Galveston, P.O. Box 1675, Galveston, Texas 77553 USA
3
Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204 USA
4
Department of Life Sciences, Texas A&M University – Corpus Christi, Corpus Christi, Texas 78412 USA
5
Stable Isotope Ecology Laboratory, Center for Applied Isotope Studies, University of Georgia, Athens, Georgia 30602 USA

Citation: Kuhn, A. L., J. S. Kominoski, A. R. Armitage, S. P. Charles, S. C. Pennings, C. A. Weaver, and T. R. Maddox.
2021. Buried hurricane legacies: increased nutrient limitation and decreased root biomass in coastal wetlands. Ecosphere
12(8):e03674. 10.1002/ecs2.3674

Abstract. Plant identity and cover in coastal wetlands is changing in worldwide, and many subtropical
salt marshes dominated by low-stature herbaceous species are becoming woody mangroves. Yet, how
changes affect coastal soil biogeochemical processes and belowground biomass before and after storms is
uncertain. We experimentally manipulated the percent mangrove cover (Avicennia germinans) in 3 × 3 m
cells embedded in 10 plots (24 × 42 m) comprising a gradient of marsh (e.g., Spartina alterniflora, Batis mar-
itima) and mangrove cover in Texas, USA. Hurricane Harvey made direct landfall over our site on 25
August 2017, providing a unique opportunity to test how plant composition mitigates hurricane effects on
surface sediment accretion, soil chemistry (carbon, C; nitrogen, N; phosphorus, P; and sulfur, S), and root
biomass. Data were collected before (2013 and 2016), one-month after (2017), and one-year after (2018)
Hurricane Harvey crossed the area, allowing us to measure stocks before and after the hurricane. The
accretion depth was higher in fringe compared with interior cells of plots, more variable in cells dominated
by marsh than mangrove, and declined with increasing plot-scale mangrove cover. The concentrations of P
and δ34S in storm-driven accreted surface sediments, and the concentrations of N, P, S, and δ34S in underly-
ing soils (0–30 cm), decreased post-hurricane, whereas the C concentrations in both compartments were
unchanged. Root biomass in both marsh and mangrove cells was reduced by 80% in 2017 compared with
previous dates and remained reduced in 2018. Post-hurricane loss of root biomass in plots correlated with
enhanced nutrient limitation. Total sulfide accumulation as indicated by δ34S, increased nutrient limitation,
and decreased root biomass of both marshes and mangroves after hurricanes may affect ecosystem func-
tion and increase vulnerability in coastal wetlands to subsequent disturbances. Understanding how
changes in plant composition in coastal ecosystems affects responses to hurricane disturbances is needed
to assess coastal vulnerability.

Key words: disturbance; Hurricane Harvey; marsh–mangrove ecotone; nutrient biogeochemistry; pulse dynamics;
sediment deposition.

Received 15 March 2021; accepted 23 March 2021; final version received 24 May 2021. Corresponding Editor: Debra P.
C. Peters.
Copyright: © 2021 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.
E-mail: jkominos@fiu.edu

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KUHN ET AL.

INTRODUCTION (Doughty et al. 2017, Charles et al. 2020).

Increased mangrove cover enhances wetland car-
A fundamental challenge in ecology is to bon storage through higher above- and below-
understand how disturbance pulses (Junk et al. ground biomass, accumulation of more
1989, Odum et al. 1995, Polis et al. 1997, Yang recalcitrant organic matter, and reduced surface
et al. 2008, 2010) and subsidy-stress gradients organic matter breakdown compared with
drive ecosystem structure and function (Odum marshes (Charles et al. 2020).
et al. 1979, Wilson et al. 2019). At the same time, Although coastal wetlands attenuate wind and
climate change is driving global redistribution of wave energy associated with storms (Danielsen
species and altering emergent properties of et al. 2005, Gedan et al. 2011, Zhang et al. 2012),
ecosystem structure and function (Walther et al. it is unclear how high-energy storms impact soil
2002, Chen et al. 2011, Lenoir and Svenning processes in wetlands of varying marsh and
2014). In coastal landscapes, climate and land- mangrove cover (Alongi 2008, Doughty et al.
use changes are transforming species composi- 2017). Hurricanes are large-scale pulsing events
tion in coastal landscapes (Day et al. 2008, Cover- driving structural and functional changes in
dale et al. 2013), as many species are expanding coastal ecosystems (Michener et al. 1997, Lugo
their ranges poleward, creating novel ecotones of 2008). In the marsh–mangrove ecotone, man-
communities in transition (Chen et al. 2011, groves generally prevent more soil erosion and
Alexander et al. 2015). Mangroves, for example, are prone to more physical damage from hurri-
are encroaching into marshes through range canes than marsh vegetation, which may limit
expansion along the temperate–tropical ecotone longer-term shoreline erosion protection (Armi-
(Cavanaugh et al. 2014, Yando et al. 2016, Kelle- tage et al. 2020). Black mangrove aboveground
way et al. 2017). In some regions, mangrove lati- regrowth can occur immediately following a hur-
tudinal expansion and contraction is strongly ricane (Armitage et al. 2020), but the impacts of
influenced by the frequency and intensity of hurricane-related stress on soil chemical concen-
extreme cold events (Osland et al. 2013, Saintilan trations and belowground processes are uncer-
et al. 2014, Coldren et al. 2019). In these transi- tain. In particular, delayed mortality has been
tional regions, small temperature changes can observed in mangroves following hurricanes
spur nonlinear expansion or contraction of man- (Radabaugh et al. 2020), suggesting that hurri-
grove forest area (Osland et al. 2017, Saintilan canes create long-lasting legacies in soils or plant
et al. 2018). Increased minimum temperature physiology.
drives mangrove expansion, whereas freeze Here, we tested how plant species identity and
events cause a dieback and reduction in man- cover in coastal wetlands at the marsh–man-
grove cover (Perry and Mendelssohn 2009, Ross grove ecotone affected surface sediment accre-
et al. 2009, Cavanaugh et al. 2014). tion and chemistry, soil chemistry, and root
Mangrove expansion into herbaceous marshes biomass before (Charles et al. 2020) and after
can alter above- and belowground soil organic Hurricane Harvey crossed directly over the
and inorganic matter concentrations. Mangroves marsh. We expected a high-magnitude hurricane
increase sediment retention and accretion, reduce such as Hurricane Harvey to transport large sedi-
erosion, attenuate waves, and increase carbon ment loads into coastal wetlands (Tweel and
and nutrient storage (Friess et al. 2011, Comeaux Turner 2012). Our analyses were guided by the
et al. 2012, Kelleway et al. 2017, Chen et al. 2018, following predictions: (1) The quantity of storm
Charles et al. 2020, Pennings et al. 2021). Man- sediment deposited during the hurricane would
grove roots stabilize the soil substrate and decrease along a gradient of mangrove cover
increase elevation, and the prevention of vertical because mangroves can attenuate allochthonous
erosion and accumulation of slower-decaying matter during events (Charles et al. 2020); (2)
organic matter increase soil carbon content in sediments transported by the storm would have
mangroves (Gedan et al. 2011, Charles et al. higher carbon and nutrient (nitrogen [N], phos-
2020). At the landscape level, increases in man- phorus [P], and sulfur [S]) concentrations than
grove cover and stand height can both attenuate pre-storm accreted sediments, as has been
and increase retention of allochthonous subsidies observed with marine wrack deposition and

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KUHN ET AL.

other storms in the Gulf of Mexico (Castañeda- randomly selected cells within the 10 plots to cre-
Moya et al. 2010, Castañeda-Moya et al. 2020, ate 10 different amounts of plant cover for the
Charles et al. 2020); (3) marshes would have whole plot: 0%, 11%, 22%, 33%, 44%, 55%, 66%,
greater chemical changes to soils than man- 77%, 88%, and 100%. Marsh vegetation naturally
groves; and (4) higher total sulfide accumulation recolonized in cells where mangroves had been
in soils as indicated by δ34S would occur where removed (Guo et al. 2017, Charles et al. 2020).
plant stress and sedimentation were highest, Some interior marsh (n = 8) and fringe man-
reflecting reduced soil conditions (Holmer and grove cells (n = 3) did not revegetate or appar-
Hasler-Sheetal 2014). We also anticipated (5) ently eroded after the hurricane. We refer to all
lower root biomass where storm-driven soil cells where mangroves were removed as marsh
nutrients increased (i.e., fringe > interior) because cells and all cells where mangroves were left
allochthonous subsidies may enhance above- intact as mangrove cells hereafter. In each plot,
ground and reduce belowground growth (Poor- we randomly sampled from four 3 × 3 m cells
ter and Nagel 2000, Deegan et al. 2012). One year along the coastal fringe (cells in the front third of
following the hurricane, we predicted that (6) the each plot, 3–9 m from the channel) and from four
lowest root biomass in plots would be where 3 × 3 m cells within the plot interior (cells in the
there was the greatest vegetation cover damage remaining two thirds of each plot). Replicate cells
(Armitage et al. 2020), because plant energy were all marsh (in the 0% mangrove plot), all
would be allocated to recovery aboveground. mangrove (in the 100% mangrove plot), or half
marsh and half mangrove (in mixed plots), that
METHODS is, two marsh and two mangrove cells in both
fringe and interior zones. We sampled a total of
Study site and experimental plots n = 80 cells.
This research was conducted in the microtidal
saline wetlands of Harbor Island, Port Aransas, Hurricane Harvey: hydrology and storm surge
Texas, USA (27.86° N, 97.06° W). Mangroves Hurricane Harvey made landfall on 25 August
have been there since at least the 1930s (Mon- 2017 directly on our site as a Category 4 hurri-
tagna et al. 2011). Mangrove expansion and con- cane (Fig. 1) with sustained hurricane-force wind
traction since the mid-1900s resulted in reversals speeds exceeding 119 kph (gusts up to 225 kph)
in dominance at the marsh–mangrove ecotone for approximately 6 h (Blake and Zelinsky 2018).
(Comeaux et al. 2012, Osland et al. 2017). The A tide gauge at Port Aransas, ~3.5 km from the
most recent mangrove expansion followed freeze experimental plots, recorded a storm surge of
events from 1980 to 1989 that caused widespread 1.6 m above MLLW (NOAA 2019), and estimates
mangrove contraction (Armitage et al. 2015). In of storm surge based on debris deposition and
2012, the wetlands were predominately occupied other flood evidence indicated a storm surge of
by black mangroves (Avicennia germinans); up to 2.4 m (USGS 2019). Major flooding (0.8 m
approximately 10% of total plant cover then was above MLLW) persisted for approximately 6 h.
marsh species (mostly Spartina alterniflora, Batis All methods and analyses in this study refer to
maritima, Salicornia, and Sarcocornia spp.; Guo three sampling periods: pre-hurricane (2013–
et al 2017). 2016; Charles et al. 2020), immediately post-
We assessed the outcome from different sce- hurricane (October 2017), and after one year of
narios of mangrove expansion and contraction recovery post-hurricane (November 2018).
by removing mangroves to create a gradient of
marsh and mangrove cover (Fig. 1). We estab- Surface sediment accretion
lished 10 large coastal plots in 2012 (24 m paral- In 2013, four years before Hurricane Harvey, we
lel to the coastline and extending 42 m inland) in randomly installed feldspar marker horizons
wetlands of similar geomorphology located (0.5 m2; Cahoon and Turner 1989) in each plot
along the Lydia Ann Shipping Channel (Guo (n = 4 marsh cells and n = 4 mangrove cells per
et al. 2017). We created 112 cells that were plot, n = 80 in total). We measured accretion depth
3 × 3 m within each of the 10 plots. We then (cm) onto feldspar marker horizons following
removed enough of the aboveground biomass in Cahoon and Turner (1989) in 2015 (pre-hurricane,

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KUHN ET AL.

Fig. 1. Aerial imagery of coastal experimental plots (indicated by white outlines) on Harbor Island, Port Ara-
nsas, Texas, USA. The percent values indicate the maintained mangrove cover of each 24 × 42 m plot (n = 10)
comprised of 3 × 3 m2 monospecific marsh or mangrove cells (n = 112 cells/plot). The red line on the map of
Texas denotes the relative path of Hurricane Harvey, which made direct landfall on our sites on 25 August 2017
as a Category 4 hurricane. Due to space limitations, graphic image of cells in each plot in the bottom panels of
the figure represents half of the actual 3 × 3 m2 cells in plots.

22 months post-installation, n = 47) and 2017 horizons were established (n = 8 per plot) to
(immediately post-hurricane, 52-months post- measure chemistry in the accreted surface sedi-
installation, n = 19). Feldspar marker horizons ments and soils. We separated the accreted sur-
could no longer be identified in 2018. face sediments from lower soil layers if feldspar
marker horizons were present. If not present,
Accreted surface sediment and soil chemistry then the entire core was treated as a soil sample
In 2015, 2017, and 2018, we collected soil cores (assuming no accreted surface sediments). We
(5 cm diameter × 30 cm depth) in each of the removed roots from the accreted surface sedi-
same randomized cells where feldspar marker ments and soils, and cores were homogenized

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KUHN ET AL.

and subsampled for chemical analyses. Subsam- root biomass ðgC=m2 Þ ¼

ples were dried at 60°C to a constant dry mass. root dry mass ðgÞ  C content ð%Þ
We ground and homogenized portions with an (1)
core area ðm2 Þ
8000-D ball mill (Spex SamplePrep, Metuchen,
New Jersey, USA). We measured the percent-
age of carbon (C) and percentage of nitrogen Data analyses
(N) using a CHN Analyzer (PerkinElmer 2400, Although a lack of spatial replication of our
Waltham, Massachusetts, USA). We determined plot-scale mangrove cover treatments violates
the percentage of phosphorus (P) using acid assumptions of inferential statistics (Hurlbert
hydrolysis followed by spectrophotometric 1984), the multiple treatment cells and plots of
analysis to estimate phosphate concentration of our experiment and inclusion of measurements
the extract (Fourqurean et al. 1992). A Thermo- from pre- and post-hurricane years were neces-
Electron Delta V Mass Spectrometer via ConFlo sary to capture integrated ecosystem-scale
III Interface (Thermo Fisher Scientific, Waltham, responses to vegetation type and cover, and hur-
Massachusetts, USA) was used to measure the ricane impacts.
%S and stable isotopes. The ratios of heavy to To test whether hurricane storm effects on
light stable isotopes are expressed as δ to indi- accreted sediments varied along a gradient of
cate relative depletion (−) or the enrichment mangrove cover in marsh and mangrove cells
(+) of the heavy isotope compared with the (predictions 1, 2), we fit linear models of accre-
lighter isotope relative to a standard, according tion depth and chemistry collected from feldspar
to the formula: δX (‰) = ([Rsample/Rstandard] − 1) marker horizons to cell-scale vegetation type
× 103, where X is 34S and R is 34S:32S. Results (marsh, mangrove) nested within continuous
are presented as deviations from a standard effects of plot-scale mangrove cover (0–100%)
(Canyon Diablo troilites for S). Repeatability pre- and post-hurricane. We used adjusted R2 to
was δ34S
0.3‰. assess goodness of fit of linear models. Variance
in post-hurricane accretion depth in marsh and
Marsh and mangrove root biomass mangrove cells was compared using Welch’s
We collected a second set of soil cores (5 cm two-sample t test.
diameter × 30 cm depth) to measure root bio- To test hurricane storm effects on the chem-
mass. Pre-hurricane (2013), we measured root istry of soils (predictions 3, 4) and root biomass
biomass in four fringe and four interior cells of (predictions 5, 6) along a gradient of mangrove
each of six of the ten plots (0%, 22%, 33%, 55%, cover in marsh and mangrove cells, we built hier-
66%, and 100% mangrove; n = 48 cells; Charles archical linear mixed-effects (LME) models using
et al. 2020). Post-hurricane (2017 and 2018), we the lme4 package in R (Bates et al. 2015). Specifi-
quantified marsh and mangrove root biomass in cally, we assessed nested factors (cell-scale vege-
four fringe and four interior cells in all 10 plots tation type [marsh, mangrove] and cell location
(n = 80 cells). We separated live roots (1–20 mm within plot [fringe, interior], and continuous
diameter) using a 1-mm mesh sieve, identified effects of plot-scale mangrove cover [0–100%]),
them as living or dead based on color, turgidity, categorical effects of hurricane (pre, post), and
and buoyancy, and collected them for root bio- random effects of year. Mixed-effects models are
mass measurements. We sorted live roots into appropriate statistical tools for analyzing data
two size classes: fine (1–6 mm diameter) and collected across multiple spatial and temporal
coarse roots (>6 mm diameter). Living roots scales (Zuur et al. 2009). We included fixed and
have been empirically identified using these random factors in models to allow us to assess
physical attributes in both marsh (Connor and independent variables and to account for hierar-
Chmura 2000) and mangrove (Komiyama et al. chical structure (spatial nestedness; Zuur et al.
1987) vegetation. We determined the organic 2009). We used conditional R2 to assess goodness
content of live roots by calculating ash-free dry of fit for mixed-effects models (includes variance
mass (loss on ignition in a muffle furnace at of fixed effects and random effects; Nakagawa
500°C for 5 h). We calculated belowground bio- and Schielzeth 2013). Due to the large number
mass using the equation from Karam (1993): of variance–covariance parameters in these

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KUHN ET AL.

complex mixed-effects models, there were some marsh and mangrove cells in all plots pre- and
instances of singular fits for random but not fixed post-hurricane (Table 2; Appendix S1: Fig. S1).
factors. Data files and model code are provided The soil N (%) decreased slightly post-hurricane
for further information (Data S1: Harvey RAPID (Table 2, Fig. 3). The soil %P decreased dramati-
Sediment Soils Roots). cally post-hurricane in all plots, especially in
All response variables were log10-transformed fringe mangrove cells and interior marsh cells
where necessary to reduce heteroskedasticity of plots in plots with lower mangrove cover
variances, and all transformed data were stan- (Table 2, Fig. 4). The soil S (%) decreased post-
dardized to z-scores to center the data and hurricane and was highly variable among inte-
enhance interpretation among continuous pre- rior and fringe marsh and mangrove cells in all
dictors (Gelman and Hill 2006). All statistical plots (Table 2; Appendix S1: Fig. S2).
analyses were performed using RStudio Despite reduction in isotopic sulfur (δ34S; ‰)
v.1.3.1093 (R Core Team 2020). concentrations in some soils post-hurricane, soil
δ34S remained oxidized in fringe and interior
RESULTS mangrove cells of plots (Table 2, Fig. 5B). More
depleted δ34S values were observed in coastal
Surface sediment accretion (fringe) marsh cells one month after the hurri-
The surface sediment accretion depth (cm) was cane (2017), and by one year post-hurricane
highest after the hurricane compared with before (2018), δ34S values were further depleted in both
the hurricane and was lower in mangrove cells marsh and mangrove fringe soils (Fig. 5A, B).
(Table 1). Accretion depth was 2.3× greater in
marsh cells than mangrove cells after the hurri- Marsh and mangrove root biomass
cane (Table 1, Fig. 2A). The accretion depth Pre-hurricane, total (coarse and fine) live root
decreased in mangrove cells with plot-scale man- biomass (0–30 cm; g C/m2) was higher in interior
grove cover before and after the hurricane and fringe mangrove cells of plots than in fringe
(Table 1, Fig. 2A). Post-hurricane cell-scale accre- marsh cells, and increased with plot-scale man-
tion depth was more variable in marsh (CV = grove cover (Fig. 6). Biomass was 1.9× higher in
72%) than mangrove cells (CV = 17%; t = 2.44, mangrove than in marsh cells and 3.7× higher in
df = 8.87, P = 0.04; Table 1, Fig. 2A). interior than in fringe cells (Fig. 6). Coarse and
fine root biomass decreased post-hurricane in
Accreted surface sediment and soil chemistry both marsh and mangrove cells and in fringe and
The concentrations of S (%) in the accreted sur- interior cells of plots (Table 2, Fig. 6).
face sediments were similar in fringe and in inte-
rior marsh and mangrove cells of all plots before DISCUSSION
and after the hurricane (Table 1, Fig. 2B). The iso-
topic sulfur (δ34S) (‰) values in accreted surface Our results indicate that although plant com-
sediments were reduced in marsh and mangrove position influenced physical processes during the
cells in all plots post-hurricane compared with hurricane, the chemistry accreted sediments and
before the hurricane (Table 1, Fig. 2C). The con- soils in marshes and mangroves were largely
centrations (%) of C and N in accreted surface reduced and homogenized by Hurricane Harvey.
sediments were greater in mangrove cells at Storm surges often bring pulses of sediments that
higher plot-scale mangrove cover both pre- and are attenuated and filtered by coastal wetlands.
post-hurricane (Table 1, Fig. 2D, E). Concentra- We expected that the storm surge from Hurri-
tions of P (%) in accreted surface sediments were cane Harvey transported large sediment loads
reduced by nearly 50% post-hurricane (Table 1, into coastal wetlands as has been observed with
Fig. 2F). other storms (Castañeda-Moya et al. 2010, Tweel
The chemical concentrations of soils (0–30 cm and Turner 2012, Castañeda-Moya et al. 2020).
below the marker horizons) were variable rela- We predicted that the aerial roots and branching
tive to cell- and plot-scale vegetation composi- stems of mangrove trees would promote more
tion and generally decreased post-hurricane. The deposition than in marsh vegetation and that the
soil %C was similar among interior and fringe quantity of storm sediment deposited during the

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KUHN ET AL.

Table 1. Linear model results of cell-scale vegetation type (marsh, mangrove) nested within continuous effects of
plot-scale mangrove cover (0–100%) from surface sediment accretion depth and accreted surface sediment
chemistry responses to Hurricane Harvey.

Model
Variable Factor Estimate SE t P Adj. R2 P

Accretion depth (cm) Intercept 0.476 0.252 1.89 0.06 0.13 <0.01
Hurricane −0.303 0.132 −2.30 0.03
Cover:Mangrove −0.009 0.004 −2.37 0.02
Cover:Marsh −0.002 0.005 −0.38 0.71
%C Intercept −0.279 0.249 −1.12 0.27 0.15 <0.01
Hurricane −0.134 0.130 −1.03 0.31
Cover:Mangrove 0.011 0.004 2.79 0.01
Cover:Marsh −0.001 0.005 −0.28 0.78
%N Intercept −0.355 0.259 −1.37 0.18 0.08 0.04
Hurricane 0.038 0.136 0.28 0.78
Cover:Mangrove 0.001 0.004 2.42 0.02
Cover:Marsh 0.001 0.006 0.11 0.91
%P Intercept −0.533 0.220 −2.43 0.02 0.34 <0.001
Hurricane 0.666 0.115 5.79 <0.001
Cover:Mangrove 0.005 0.003 1.57 0.12
Cover:Marsh 0.004 0.005 0.84 0.41
%S Intercept −0.105 0.260 −0.41 0.69 0.07 0.05
Hurricane −0.078 0.136 −0.57 0.57
Cover:Mangrove 0.006 0.004 1.65 0.11
Cover:Marsh −0.005 0.006 −0.85 0.40
δ34S (‰) Intercept −0.386 0.194 −1.99 0.05 0.49 <0.001
Hurricane 0.765 0.102 7.54 <0.001
Cover:Mangrove 0.002 0.003 0.77 0.45
Cover:Marsh −0.001 0.004 −0.22 0.83
Notes: Bolded values denote significance of P < 0.05 using α = 0.05.
SE, standard error. Adjusted R2 was used to assess goodness of fit for models for each parameter. Samples were collected
from 0.5-m2 feldspar marker horizons that were established in 2013 in marsh and mangrove cells in plots (n = 10) that span a
gradient in percent mangrove cover (0%, 11%, 22%, 33%, 44%, 55%, 66%, 77%, 88%, and 100%). Data from pre-hurricane were
collected in 2015 (n = 47 total; see Charles et al. 2020). Data from post-hurricane were collected in 2017 (n = 19). Feldspar mark-
ers could not be located in 2018.

hurricane would increase along a gradient of [nitrogen (N), phosphorus (P), and sulfur (S)]
plot-scale mangrove cover. However, these pre- content than pre-storm accreted sediments (Cas-
dictions were not fully supported. Instead, storm tañeda-Moya et al. 2010) and (2) marshes would
surge sediment accretion was highest and most have greater chemical changes to accreted sur-
variable in marsh cells and decreased in man- face sediments and soils than mangroves were
grove cells with plot-scale mangrove cover partially supported. We measured reduced nutri-
(Table 1). Relative to the marsh cells, mangrove ent, but not carbon concentrations, in accreted
cells likely promoted autochthonous sediment surface sediments and soils, and these persisted
retention and may have inhibited storm-driven one year after the hurricane. We anticipated a
sediment deposition and erosion (Armitage et al. high sulfide (δ34S) accumulation, as indicated
2020, Charles et al. 2020, Pennings et al. 2021). from depleted δ34S content in accreted surface
Our observations suggest that mangroves trap sediments and soils, where plant stress and sedi-
debris at the very front of plots and of mangrove mentation reduced soil conditions (Holmer and
cells and that this likely inhibited the transport of Hasler-Sheetal 2014), which we observed in
allochthonous sediments into and through areas marsh cells across plot-scale mangrove cover,
with high mangrove cover (Guo et al. 2017). Our especially in the eroded fringes of plots (Armi-
predictions that (1) storm-driven sediment accre- tage et al. 2020, Pennings et al. 2021). We pre-
tion would have higher carbon and nutrient dicted lowest root biomass in treatments of

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KUHN ET AL.

Fig. 2. Measured surface sediment accretion (cm; A) and its chemical concentrations (%S, B; δ34S, ‰, C; %C,
D; %N, E; and %P, F) from coastal wetland plots in Port Aransas, Texas, USA, from dates pre- (2013) and post-
Hurricane Harvey (2017). Symbols correspond to wetland cells (3 × 3 m) of different vegetation types (marsh,
open; mangrove, filled) along a gradient in plot-level percent mangrove cover.

greatest vegetation cover damage (Armitage differentially modify soil strength through
et al. 2020), but there was a coincidental wide- organic detritus input, and greater root biomass
spread depletion in δ34S and lower root biomass and organic content in these mangrove cells
across both marsh and mangrove cells in all (Charles et al. 2020), and may lower soil bulk
plots. density and increase sediment stability (Feagin
Sediment deposition by hurricanes into coastal et al. 2009). Our research suggests that man-
wetlands is well documented (Nyman et al. 1995, groves function as critical biophysical filters on
Cahoon et al. 1996) and may enhance surface ele- multiple spatial scales despite storm-driven
vation and carbon burial relative to eustatic sea changes in sediment biogeochemistry, retaining
level rise (McKee and Cherry 2009, Smoak et al. accreted sediments along coastal fringe margins
2013, Baustian and Mendelssohn 2015). Sediment (Charles et al. 2020) and reducing sediment even
deposition may bury mangrove and marsh roots at low plot-scale mangrove cover (Pennings et al.
(Ellison 1999, Macreadie et al. 2013) depending 2021). Increases in mangrove cover in coastal
on geomorphic setting, hurricane path, and type wetlands may therefore enhance physical shore-
of sediment deposited (Smith et al. 2009). How- line retention and reduce storm sediment and
ever, in our study, mangrove cells inhibited sur- wrack deposition (Armitage et al. 2020, Pennings
face sediment accretion post-hurricane. Results et al. 2021).
from other studies in these same wetlands found Although mangroves provided shoreline pro-
that mangrove cover enhanced shoreline reten- tection through reduced erosion, hurricane storm
tion by reducing vertical and fringe erosion, surge increased nutrient limitation and stress in
which is likely attributed to greater soil strength both marshes and mangroves. Soils in this region
in mangrove cells (Armitage et al. 2020, Pennings are primarily inorganic and sand-rich (7% C con-
et al. 2021). Coastal vegetation species tent) with higher organic content in mangrove

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KUHN ET AL.

Table 2. Hierarchical linear fixed-effects model outputs comparing nested factors (cell-scale vegetation type
[marsh, mangrove] and cell location within plot [fringe, interior], and continuous effects of plot-scale man-
grove cover [0–100%]), categorical effects of hurricane (pre, post), and random effects of year from soil (0–
30 cm) chemistry and total live root biomass responses to Hurricane Harvey.

Variable Factor Estimate SE df t P Model conditional R2

Soil %C Intercept −0.032 0.225 5.06 −0.14 0.89 0.12

Hurricane 0.100 0.194 2.78 0.52 0.64
Cover:Fringe:Mangrove 0.004 0.003 182.97 1.32 0.19
Cover:Interior:Mangrove 0.003 0.003 182.92 0.99 0.32
Cover:Fringe:Marsh −0.001 0.004 183.34 −0.32 0.75
Cover:Interior:Marsh −0.003 0.004 182.87 −0.95 0.35
Soil %N Intercept 0.022 0.143 5.06 −0.14 0.89 0.13
Hurricane 0.329 0.088 2.06 3.75 0.06
Cover:Fringe:Mangrove 0.003 0.003 182.70 1.24 0.22
Cover:Interior:Mangrove 0.001 0.003 182.40 0.42 0.68
Cover:Fringe:Marsh −0.001 0.004 184.20 −0.22 0.83
Cover:Interior:Marsh −0.004 0.004 182.20 −1.05 0.30
Soil %P Intercept 0.157 0.082 186.00 1.91 0.06 0.69
Hurricane 0.800 0.043 186.00 18.78 <0.001
Cover:Fringe:Mangrove 0.003 0.002 186.00 2.11 0.04
Cover:Interior:Mangrove −0.003 0.002 186.00 −1.94 0.05
Cover:Fringe:Marsh 0.004 0.002 186.00 0.17 0.86
Cover:Interior:Marsh −0.006 0.002 186.00 −2.52 0.01
Soil %S Intercept 0.273 0.136 186.00 2.01 0.05 0.09
Hurricane 0.266 0.070 186.00 3.78 <0.001
Cover:Fringe:Mangrove −0.004 0.003 186.00 −1.52 0.13
Cover:Interior:Mangrove −0.004 0.003 186.00 −1.41 0.16
Cover:Fringe:Marsh −0.004 0.004 186.00 −1.22 0.23
Cover:Interior:Marsh −0.007 0.004 186.00 −1.93 0.06
Soil δ34S (‰) Intercept −0.330 0.137 186.00 −2.40 0.02 0.07
Hurricane −0.003 0.071 186.00 −0.04 0.96
Cover:Fringe:Mangrove 0.009 0.003 186.00 3.26 0.001
Cover:Interior:Mangrove 0.007 0.003 186.00 2.59 0.01
Cover:Fringe:Marsh 0.001 0.004 186.00 0.40 0.69
Cover:Interior:Marsh 0.006 0.004 186.00 1.73 0.09
Fine root biomass (g C/m2) Intercept 0.062 0.111 30.27 0.56 0.58 0.32
Hurricane 0.506 0.073 6.01 6.98 <0.001
Cover:Fringe:Mangrove 0.005 0.002 190.57 2.04 0.04
Cover:Interior:Mangrove 0.012 0.002 190.57 5.09 <0.001
Cover:Fringe:Marsh −0.008 0.003 190.64 −2.69 <0.01
Cover:Interior:Marsh 0.006 0.003 190.62 1.99 0.05
Coarse root biomass (g C/m2) Intercept 0.418 0.141 129.00 2.95 <0.01 0.51
Hurricane 0.837 0.077 129.00 10.85 <0.001
Cover:Fringe:Mangrove 0.003 0.002 129.00 1.02 0.31
Cover:Interior:Mangrove 0.002 0.002 129.00 1.09 0.28
Cover:Fringe:Marsh 0.001 0.004 129.00 0.38 0.70
Cover:Interior:Marsh −0.005 0.004 129.00 −1.28 0.20
Notes: Bolded values denote significance of P < 0.05 using α = 0.05.
SE, standard error. Conditional R2 was used to assess goodness of fit for linear mixed-effects models (includes variance of
fixed effects and random effects; Nakagawa and Schielzeth 2013). A total of n = 80 soil cores were collected and analyzed. Data
from pre-hurricane were collected in 2013 (see Charles et al. 2020). Data from post-hurricane were collected in 2017 and 2018.
We report the mean value from post-hurricane years, except for δ34S which changed from 2017 to 2018. Model results include
significant (α = 0.05) terms and overall model fit (conditional R2 values and P values). When one vegetation type (marsh, man-
grove) and/or cell location (fringe, interior) was significant, the category was specified in the table. Only vegetation type (marsh,
mangrove) and/or cell location (fringe, interior) was specified in the table when both types were significant.

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KUHN ET AL.

Fig. 3. Nitrogen (N) content (%) in soils (0–30 cm

below marker horizons) from coastal wetland plots in
Port Aransas, Texas, USA, from dates pre- (2013) and Fig. 4. Phosphorus (P) content (%) in soils (0–30 cm
post-Hurricane Harvey (2017, 2018). Boxplots corre- below the marker horizon) from coastal wetland plots
spond to (A) wetland cells (3 × 3 m) of different vege- in Port Aransas, Texas, USA, from dates pre- (2013)
tation type (marsh, gray; mangrove, black) along a and post-Hurricane Harvey (2017, 2018). Boxplots cor-
gradient in plot-level percent mangrove cover and (B) respond to (A) wetland cells (3 × 3 m) of different veg-
fringe or interior locations of plots. etation types (marsh, gray; mangrove, black) along a
gradient in plot-level percent mangrove cover and (B)
fringe or interior locations of plots.
than in marsh cells (Charles et al. 2020). We pre-
dicted that suspended marine sediments deliv- chemical concentrations in surface accreted sedi-
ered by storm surge would supply a nutrient ments decreased (%P) or were similar (%N, %S)
pulse (Nyman et al. 1995, Davis et al. 2004, Cas- from pre- to post-hurricane across vegetation
tañeda-Moya et al. 2010) in the accreted surface treatments. Our findings diverge from previous
sediment that could increase root growth (McKee studies in the Gulf of Mexico that have measured
and Cherry 2009). Contrary to these hypotheses, increased sediment P concentrations in marine

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KUHN ET AL.

elevation and sediment nutrient content (Cas-

tañeda-Moya et al. 2010, 2020). Prior to Hurricane
Harvey, C and nutrients in accreted sediments
were greater in mangrove than in marsh cells
(Charles et al. 2020), but post-hurricane reductions
in sediment nutrient concentrations and similarity
between mangroves and marshes suggest that
there was erosion of surficial sediment and soils
followed by storm surge deposition of organic-
and nutrient-poor sediments. In addition, the
source and nutrient content of sediments determi-
nes whether sediments deposited by storms repre-
sent a subsidy or stress (Smith et al. 2009,
Castañeda-Moya et al. 2010, Radabaugh et al.
2020). The reduction in %P and depletion in δ34S
in sediment and soil following Hurricane Harvey
could partially explain reductions in root biomass
in all wetlands. Our results indicate that storm
surge sediments that are low in organic matter
and nutrient content function more as a stress than
a subsidy to hurricane-impacted wetlands through
root burial and increased nutrient limitation.
Storm sedimentation is complex and drives
heterogeneous responses in coastal vegetation. For
example, sedimentation can interfere with gas
exchange and nutrient cycling in wetland roots
and soil (Lugo et al. 1981, Radabaugh et al. 2020),
and delayed mangrove responses to hurricanes
have been documented elsewhere along the Gulf
Coast. After the passage of a Category 4 hurricane
over the Florida Keys, mangrove island trees
(A. germinans and others) suffered delayed mortal-
ity after nine months, which was attributed to root
burial by storm surge deposits (Radabaugh et al.
2020). After the passage of Hurricane Wilma over
the Florida Everglades, mangrove mortality, root
Fig. 5. δ34S content (‰) in soils (0–30 cm below loss, and soil substrate compaction were observed
marker horizons) from coastal wetland plots in Port for up to three years despite leaf regrowth (Barr
Aransas, Texas, USA, from dates pre- (2013) and post- et al. 2012). Thus, although plants may recover
Hurricane Harvey (2017, 2018). Boxplots correspond aboveground from hurricanes, belowground bur-
to (A) wetland cells (3 × 3 m) of different vegetation dens through reduced soil nutrients and root bio-
types (marsh, gray; mangrove, black) along a gradient mass can impact holistic recovery of coastal
in plot-level percent mangrove cover and (B) fringe or wetlands. However, long-term responses to
interior locations of plots. hurricane-induced sedimentation have shown dis-
tinct periods of elevation loss followed by eleva-
sediment deposits from hurricane storm surge. tion gain driven by surface and subsurface
For example, storm surge from Hurricane Wilma processes (Feher et al. 2020). Further, the timing of
in the Florida Everglades increased sediment storm surge can influence whether it is detected as
accretion in tidal riverine mangrove forests by a relative subsidy or stress. Recent evidence in
17× compared with annual vertical accretion marsh–mangrove ecotones, for example, illustrates
rates, contributing to a net gain in surface the importance of wrack in facilitating mangrove

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KUHN ET AL.

Fig. 6. Root biomass (g C/m2; 0–30 cm below marker horizons) from coastal wetland plots in Port Aransas,
Texas, USA, on dates pre- (2013) and post-Hurricane Harvey (2017, 2018). Boxplots correspond to (A, C) wetland
cells (3 × 3 m) of different vegetation types (marsh, open; mangrove, filled) along a gradient in plot-level percent
mangrove cover and (B, D) fringe or interior locations of plots.

propagule establishment into open marsh patches, biomass stocks may partially reflect plant energy
which can be inhibited if storm surge pushes reallocation to regrowth aboveground following
wrack out of critical and into marginal habitats wind defoliation and cover damage (Radabaugh
(Smith et al. 2020). et al. 2020). However, defoliation was only com-
A comprehensive understanding of above- mon in the front of the plots, whereas root bio-
and belowground recovery from hurricanes is mass loss occurred in both the fringe and interior
needed in order to assess coastal wetland vulner- of plots, indicating that reallocation of energy
ability to disturbances. According to a concur- was not the only factor explaining decreases in
rent study quantifying damage by Hurricane root biomass. Rather, our findings suggest that
Harvey to our experimental sites, black man- nutrient limitation stress and sustained storm
grove canopy cover in our plots decreased >20% surge inundation may collectively cause root bio-
from 2015 to 2017, presumably due to hurricane mass loss in wetland plants lasting more than a
wind effects, with greatest defoliation observed year post-hurricane. Results from our study are
in tall trees (>1.5 m) along the plot fringe (Armi- most applicable to arid coastal wetlands of the
tage et al. 2020) that were not submerged by the Western Gulf of Mexico, where succulent marsh
storm surge and thereby protected from winds. vegetation (e.g., Batis) dominates rather than
Mangrove recovery was observed within weeks S. alterniflora (Osland et al. 2016, Yando et al.
(Armitage et al. 2020), and reduction in root 2016). Grasses such as S. alterniflora have very

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KUHN ET AL.

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Funding was provided by a Hurricane Harvey Cahoon, D., and R. E. Turner. 1989. Accretion and canal
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