Nutrient enrichment intensiﬁes hurricane impact in scrub ...376158/UQ376158_fulltext.p… · 2006, Ridler et al. 2006, Sallenger et al. 2006, Steward et al. 2006, Tomasko et al

Ecology, 96(11), 2015, pp. 2960–2972� 2015 by the Ecological Society of America

Nutrient enrichment intensifies hurricane impact in scrubmangrove ecosystems in the Indian River Lagoon, Florida, USA

ILKA C. FELLER,1,4 EMILY M. DANGREMOND,1 DONNA J. DEVLIN,2 CATHERINE E. LOVELOCK,3 C. EDWARD PROFFITT,2

AND WILFRID RODRIGUEZ1

1Smithsonian Environmental Research Center, Smithsonian Institution, 647 Contees Wharf Road, Edgewater, Maryland 21037 USA2Department of Biological Sciences, Charles E. Schmidt College of Science, Florida Atlantic University,c/o Harbor Branch Oceanographic Institution, 5775 Old Dixie Highway, Fort Pierce, Florida 34946 USA

3Centre for Marine Studies/School of Integrative Biology, University of Queensland, St Lucia, Queensland 4072 Australia

Abstract. Mangroves are an ecological assemblage of trees and shrubs adapted to grow inintertidal environments along tropical, subtropical, and warm temperate coasts. Despiterepeated demonstrations of their ecologic and economic value, multiple stressors includingnutrient over-enrichment threaten these and other coastal wetlands globally. These ecosystemswill be further stressed if tropical storm intensity and frequency increase in response to globalclimate changes. These stressors will likely interact, but the outcome of that interaction isuncertain. Here, we examined potential interaction between nutrient over-enrichment and theSeptember 2004 hurricanes. Hurricanes Frances and Jeanne made landfall along Florida’sIndian River Lagoon and caused extensive damage to a long-term fertilization experiment in amangrove forest, which previously revealed that productivity was nitrogen (N) limited acrossthe forest and, in particular, that N enrichment dramatically increased growth rates andaboveground biomass of stunted Avicennia germinans trees in the interior scrub zone. Duringthe hurricanes, these trees experienced significant defoliation with three to four times greaterreduction in leaf area index (LAI) than control trees. Over the long term, theþN scrub treestook four years to recover compared to two years for controls. In the adjacent fringe andtransition zones, LAI was reduced by .70%, but with no differences based on zone orfertilization treatment. Despite continued delayed mortality for at least five years after thestorms, LAI in the fringe and transition returned to pre-hurricane conditions in two years.Thus, nutrient over-enrichment of the coastal zone will increase the productivity of scrubmangroves, which dominate much of the mangrove landscape in Florida and the Caribbean;however, that benefit is offset by a decrease in their resistance and resilience to hurricanedamage that has the potential to destabilize the system.

Key words: coarse woody debris; delayed mortality; disturbance; Florida; growth rate; hurricane;Indian River Lagoon; leaf area index; mangrove forest; nutrient enrichment; resilience; resistance.

INTRODUCTION

Hurricanes are a frequent but aperiodic natural form

of disturbance along coastal regions around the world.

In Florida and throughout much of the Caribbean, these

episodic storms have direct and indirect effects on the

dynamics of mangrove forests, which dominate coastal

landscapes in this region (Lugo 2008, Smith et al. 2009,

Jiang et al. 2014). The initial damage to mangroves and

subsequent recovery time depend not only on hurricane

intensity (e.g., wind speed, forward speed, and storm

surge), but also on forest structure, including stand

density, tree height, and biomass accumulation (Roth

1992, Doyle and Girod 1997, Piou et al. 2006, Ross et al.

2006). In mangroves, such structural characteristics also

vary in undisturbed forests along environmental gradi-

ents in tidal elevation, salinity, and nutrient availability

(Lugo and Snedaker 1974, Sherman et al. 2001, Ball

2002, Feller et al. 2003a, b, Castaneda-Moya et al. 2013).

During recovery, these characteristics can be influenced

by huge allochthonous subsidies of nutrients delivered to

mangrove forests by hurricanes (Scatena et al. 1996,

Silver et al. 1996, Davis et al. 2004, Lovelock et al.

2011).

The mangrove forests that line the Atlantic coast of

Florida were hit by more than 100 hurricanes between

1851 and 2004 (Blake et al. 2005), but multiple storms

hitting the same area of coast in a given season are

extremely rare events (Liu 2007). However, two of the

four hurricanes that hit Florida in 2004 made landfall

within ;3 km of each other along the Indian River

Lagoon (IRL) and followed nearly identical paths across

the state. Hurricane Frances, a Category 2 storm (Saffir-

Simpson Hurricane Wind Scale [NHC 2012]), came

ashore near Stuart on 5 September (Bevan 2014) with

167 km/h maximum sustained winds. It was among the

Manuscript received 1 October 2014; revised 17 April 2015;accepted 21 April 2015; final version received 13 May 2015.Corresponding Editor: R. A. Dahlgren.

4 E-mail: [email protected]

2960

10 costliest storms that have hit the United States, with

much of the damage attributed to its slow movement

(data available online).5 Three weeks later, on 25

September, Hurricane Jeanne, a Category 3 storm,made landfall near Stuart with maximum sustained

winds near 195 km/h. In the year following these storms,

several studies examined the damage to Florida’s coastal

ecosystems (e.g., Lapointe et al. 2006, Paperno et al.

2006, Ridler et al. 2006, Sallenger et al. 2006, Steward etal. 2006, Tomasko et al. 2006, Wang and Horwitz 2007,

Dix et al. 2008, Carlson et al. 2010). These studies found

spatial variation in the amount of physical damage

sustained by coastal environments and the resident flora

and fauna (Greening et al. 2006). In mangrove forests,the physical damage and level of defoliation varied with

distance from the eye walls of the hurricanes (Milbrandt

et al. 2006, Tomasko et al. 2006). Mangrove stands with

larger mangrove trees and lower densities sustained

greater damage from hurricane winds (Vogt et al. 2011).In addition, Proffitt et al. (2006) found that, in the first

year following the storms, mangrove reproduction was

reduced by an order of magnitude. However, no studies

have subsequently reported on mangrove recovery over

the longer term after hurricanes Frances and Jeanne.

Our specific objective was to investigate how differ-ences in nutrient availability affected damage levels and

long-term recovery in a mangrove forest along the IRL

following hurricanes Frances and Jeanne. These storms

passed directly over an established fertilization experi-

ment in which we had measured forest structure andtracked mangrove response to nutrient enrichment. The

initial purpose of this experiment was to examine what

types of changes occur within mangrove ecosystems in

response to nutrient over-enrichment, which remains

one of the major global threats to coastal wetlands (e.g.,Cloern 2001, Boesch 2002, Deegan et al. 2012). Results

from our experiments have previously shown that

primary production in mangrove forests along the IRL

was nitrogen (N) limited and that N enrichment

significantly altered plant growth, photosynthesis rates,tree height, leaf area index, foliar nutrient dynamics,

herbivory, decomposition, and competitive interactions

among mangrove species (Table 1; Feller et al. 2003b,

2010, 2013, Lovelock and Feller 2003). However, these

studies also showed that the size of the response to Nenrichment varied by species and zone along a tidal

elevation gradient. In the present study, we used that

fertilization experiment to determine how increased

nutrient availability and forest zone affected the

susceptibility of mangrove to hurricane damage (resis-tance) and their rate of recovery (resilience) after the

storm.

The 2004 hurricanes struck our study site eight years

after we had initiated the fertilization experiment,

providing an additional opportunity to assess the role

of disturbance in modulating growth, canopy dynamics,

and recovery. Because N was found to be the elementlimiting mangrove growth at our site, we hypothesized

that the N-fertilized (þN) trees would sustain greaterdamage than control trees as a result of decreasedresistance to hurricane winds due to larger, denser

canopies, but that they would recover faster as a resultof increased resilience associated with more rapid

growth rates (Herbert et al. 1999). We further hypoth-esized that damage and recovery would also vary byspecies and zone. Although some studies found that

susceptibility to hurricane damage varies with speciesand size of mangrove (Baldwin et al. 1995, Imbert et al.

1996, McCoy et al. 1996, Sherman et al. 2001, Vogt et al.2011), others found similar levels of damage amongmangrove species and among size classes within species

(Odum et al. 1982, Gresham et al. 1991, Smith et al.1994, Sherman et al. 2001). Because mangrove forests

are often characterized by low floristic diversity, severalstudies have predicted that the recovery trajectory isrelatively simple such that biological diversity, forest

structure, ecosystem processes, and ecological functionswill completely regain their former states followinghurricane disturbance (Lugo et al. 1976, Ogden 1992,

Smith et al. 1994). Although mangrove species diversityis low in the Atlantic-Caribbean region, the physiogno-

my of mangrove forest types is diverse, ranging fromscrub stands ,1.5 m tall to .30 m tall in riverinesystems as a function of hydrogeomorphology (Rivera-

Monroy et al. 2004). Long-term studies followingcumulative damage and recovery from multiple storms

across south Florida found that hurricane damage wasmost significantly related to forest type such that basinmangroves suffered more damage than riverine or island

mangroves while other studies observed that scrubforests showed little if any damage following even

catastrophic hurricanes (Lugo 1997, Ross et al. 2006,Smith et al. 2009). Ross et al. (2006) proposed that suchdifferences in mangrove forest type and productivity

along hydrogeomorphic gradients may arise throughcompetitive interactions that develop during recovery

following hurricane damage, suggesting a long-term

TABLE 1. Summary of growth responses of fertilized Avicenniagerminans (scrub and transition zones) and Rhizophoramangle (fringe zone) trees at Mosquito Impoundment 23(MI 23), Avalon State Park, North Hutchinson Island,Florida, USA, prior to the September 2004 hurricanes.

NutrientTreatment

Growth (cm/month)

Scrub Transition Fringe

Control 0.13 6 0.03 0.42 6 0.08 0.48 6 0.11þN 2.60 6 0.22 4.18 6 2.34 2.06 6 0.80þP 0.41 6 0.11 0.57 6 0.19 0.32 6 0.08

Notes: Growth is measured as shoot elongation in responseto nutrient enrichment with nitrogen (þN) as urea, phosphorus(þP) as triple superphosphate, or controls (no fertilizer added).Measurements are based on annual increases to individualshoots after two years of treatment (data from Feller et al.[2003b]).

5 http://www.hurricanediscovery.org/history/storms/2000s/frances/

November 2015 2961N ENRICHMENT INCREASES HURRICANE IMPACT

imprint of hurricanes on mangrove communities of the

region.

MATERIALS AND METHODS

Study site

Our study was conducted at Mosquito Impoundment

23 (MI 23), a 122-ha stand of coastal mangroves located

in the Avalon State Recreation Area on the lagoonal

side of North Hutchinson Island, St. Lucie County,

Florida, USA (278330 N, 808200 W; see Plate 1). This

impoundment was constructed in 1966 to control

populations of nuisance insects, and was maintained

until 1974 when its dike was breached (Carlson et al.

1983, Rey et al. 1986, 1990, 1992, Rey and Kain 1991).

Hydrological connection between MI 23 and the IRL is

maintained through the breach and three culverts.

Vegetation at this site is characterized by a tree-height

gradient, perpendicular to the shoreline (Fig. 1).

Rhizophora mangle L. (red mangrove) trees, 3–5 m tall,

dominate to form a dense fringe along the canal at the

seaward edge of MI 23. Landward of the fringe, the

transition zone is a mix of slender Avicennia germinans

L. (black mangrove) and Laguncularia racemosa

Gaertn.f. (white mangrove) trees of decreasing height,

from ,3.0 to .1.5 m tall. Landward of the transition

zone, the scrub zone in the interior of MI 23, is

dominated by stunted, ,1.5 m tall, old-growth A.

germinans trees characterized by low stature, infrequent

branching, and small internodal lengths (Lugo and

Snedaker 1974, Lugo 1997), which distinguishes them

from saplings, which also have low stature but are

relatively young, vigorously growing plants as indicatedby long internodes and frequent axial branching (Feller

and Mathis 1997). At MI 23, scrub A. germinans cover

over 60% of the mangrove landscape (Feller et al.

2003b).

Experimental design

The experimental design was a randomized complete

block with a factorial treatment arrangement. Transects

along the tree-height gradient were replicated in threeblocks, 100–150 m apart, along the western side of MI

23. In each block, three transects, 25–50 m long and ;10

m apart, were oriented perpendicular to the shoreline

and subdivided into fringe, transition, and scrub zones

(Feller et al. 2003b). Two species were targeted for

fertilizer treatment: R. mangle in the fringe zone and A.

germinans in the transition and scrub zones. In each

block, three replicate trees were selected within each

zone. Trees were fertilized with 300 g of N fertilizer asurea (45:0:0), or P fertilizer as P2O5 (0:45:0), as described

in Feller (1995). Nutrient treatment for each transect

within each block was assigned randomly. Nine trees per

nutrient treatment per zone in each block for a total of

81 trees (3 nutrient treatments 3 3 zones 3 3 blocks 3 3

replicate trees per zone) were treated and measured

before and after the hurricanes at six-month intervals

from 1997 to 2011. Doses (150 g) of fertilizer were

placed in small holes (3 cm diameter 3 30 cm deep),

FIG. 1. Profile of the tree-height gradient across the mangrove forest at Mosquito Impoundment 23 (MI 23), Avalon StatePark, North Hutchinson Island, St. Lucie County, Florida, USA based on point-centered quarter transects (N ¼ 4). Data fromFeller et al. (2003b).

ILKA C. FELLER ET AL.2962 Ecology, Vol. 96, No. 11

cored into the substrate beneath the drip line on

opposing sides of the canopy of each tree, and sealed.

We used this method rather than surface broadcasting to

minimize our nutrient footprint and to assure that the

fertilizers were available to tree roots rather than lost in

tidal flushing. For controls, holes were cored and sealed,

but no fertilizer was added.

Plant growth.—As a bioassay of the effects of storm

damage and nutrient treatment on plant growth, we

tracked the responses of five, initially unbranched,

shoots (first order) in sunlit positions in the outer part

of the canopy of each tree for two years following the

September 2004 hurricanes. In June 2007, about three

years after Hurricanes Frances and Jeanne, we harvested

the tagged shoots and measured shoot length and

biomass, number of nodes, and leaf area and biomass.

These data were used to determine growth rates in the

fertilization experiment.

Damage and recovery.—Damage and recovery of the

mangrove canopy structure were quantified with leaf

area index (LAI) using a gap fraction method.

Hemispherical photographs were taken with a Nikon

Coolpix digital camera (model 995; Nikon, Tokyo,

Japan) fitted with a fisheye lens and in the same

position under the canopy of each of the fertilized trees

in the experiment (Fig. 2). Images were processed using

Hemiview Canopy Analysis Software (version 2.1;

Delta-T Devices, Cambridge, UK). Pre-hurricane

LAI values were measured based on hemispherical

photographs taken in April 2003. To quantify the

damage caused by each storm, additional hemispher-

ical photographs were taken one week after Hurricane

Frances and one week after Hurricane Jeanne. To

track recovery, this process was repeated at ;6–12

month intervals thereafter for six years. At each time,

we also measured tree height and porewater salinity.

Porewater was collected from a depth of 15 cm at the

base of each tree with a probe attached to a suction

device.

Woody debris.—The input of biomass of downed and

standing woody debris as a result of the September 2004

hurricanes was quantified using 4 3 4 m plots in fringe,

transition, and scrub (N ¼ 3) zones at MI 23. The nine

plots were initially sampled in April 2005, approximately

seven months after hurricanes Frances and Jeanne. To

track changes in the amount of dead wood over the

subsequent five-year period, these plots were resampled

in June 2007 and November 2010. Each time, all pieces

of dead wood on the ground (downed) and in the

canopy (standing) were removed and sorted. After

sorting to species, samples were sorted by size class into

fine woody debris (FWD), which included twigs and

small branches (,1 cm diameter), pneumatophores,

seedlings, and coarse woody debris (CWD), which

included larger branches, boles, and prop roots (.1

cm). These samples were further sorted into three decay

classes (i.e., sound, intermediate, rotten), following the

methods described in Krauss et al. (2005). The ‘‘sound’’

class was recently killed wood with intact bark and was

indicative of dead wood caused by the September 2004

hurricanes. Both the intermediate and rotten classes had

been dead longer than one year. For the intermediate

class, the wood was still firm but was missing its bark.

For the rotten class, the wood was soft and disintegrat-

ing. All samples were then weighed, and a subsample

from each sorted component was oven-dried to deter-

mine a conversion factor for estimating dry weight per

sample, which was used for estimating biomass of

woody debris (g/m2) by species and size/decay classes.

Statistics.—Our data from the fertilization experiment

were grouped by nutrient treatment (Control, þN, þP)and zone (fringe, scrub) at three replicate sites at MI 23.

We used the GLM procedure repeated-measures anal-

ysis of variance (ANOVA) univariate tests of hypotheses

for within-subject effects on LAI measurements repeated

at 6–12 month intervals to look for possible differences

in recovery patterns over a seven-year period. We used

two-way ANOVAs for each response variable. Tukey’s

FIG. 2. Examples of the hurricane damage to the mangrove canopy at the same position in the transition zone one week afterHurricane Frances and Hurricane Jeanne and after six years of recovery.


Honestly Significant Difference (HSD) tests were

applied to examine pairwise differences within and

among the treatment levels. Response variables were

either log- or square-root transformed prior to ANOVA

analyses to respect variance homogeneity and normality.

Repeated-measures ANOVAs were done with R soft-

ware 2.9.0 (R Development Core Team 2009); all other

analyses were done in SYSTAT 11 (Systat 2004).

RESULTS

Plant growth.—Shoot elongation rates (cm/month),

which were measured four times between June 2000 and

January 2007, were used to compare plant growth before

and after the September 2004 hurricanes. The hurricanes

had a significant effect on shoot elongation over that

time period (repeated-measures ANOVA, F4,48 ¼ 33.56,

P , 0.001; Fig. 3). Before the hurricanes, the þNtreatment caused a significant increase in growth relative

to both control andþP treatment in each zone (repeated-

measures ANOVA, F2,51¼ 20.291, P , 0.001), with the

highest rates in þN trees in the transition zone trees

(repeated-measures ANOVA, F4,51¼ 4.403, P , 0.005).

For almost three years after the hurricanes, growth rates

in all zones were significantly lower than they were

before the storms, with no significant difference among

nutrient treatment levels (repeated-measures ANOVA,

F16, 147¼ 2.537, P , 0.002). Although there was a slight

but non-significant increase in growth for theþN trees in

the transition zone, values were still less than half their

pre-hurricane levels.

Leaf area index.—LAI values for individual trees in

the fertilization experiment at MI 23, which were made

11 times beginning with pre-hurricane conditions in

April 2003 through November 2011, provide a measure

of the defoliation caused by each of the storms and the

subsequent recovery of the canopy by nutrient treatment

and zone (Fig. 4). Over this time period, LAI changed

significantly (Table 2). That change in LAI over time

FIG. 3. Changes in growth rates based on shoot elongation (cm/month) of fertilized trees in scrub, transition, and fringe zonesat MI 23 before and after the September 2004 hurricanes.

FIG. 4. Damage and recovery of the mangrove canopy structure following the September 2004 hurricanes were determined withleaf area index (LAI), based analysis of hemispherical photographs of the canopy using Hemiview Canopy Analysis Software. Alldata are from 1 January.


was significantly affected by both nutrient treatment and

zone, with a significant zone 3 nutrient treatment

interaction. Although Hurricane Jeanne was the stron-

ger of the two storms, most of the reduction in LAI was

caused during Hurricane Frances, the first of the two

storms (Fig. 4). Pre-hurricane LAI levels from April

2003 showed a significant relationship with LAI

measured immediately after Hurricane Frances (r2 ¼0.45, F1,78 ¼ 64.50, P , 0.0001), but not with LAI

measured immediately after Hurricane Jeanne (P .

0.05). But, the magnitude of the effect was not uniform.

Before the storms in 2003, the effect of nutrient

treatment differed significantly by zone with a statisti-

cally significant interaction between nutrient treatment

and zone (ANOVA, F4,71 ¼ 10.54, P , 0.001). Pairwise

contrasts indicated that the LAI values for control trees

were significantly lower in the scrub zone than in the

fringe (Tukey’s HSD test, P , 0.001) or transition

(Tukey’s HSD test, P , 0.001) zones. Also within the

scrub zone,þN trees had significantly greater LAI levels

than control (Tukey’s HSD test, P , 0.001) or þP(Tukey’s HSD test, P , 0.001) trees. However,

following the September 2004 hurricanes, LAI was

reduced to similar levels in all zones.

In the scrub zone, LAI levels were reduced by 46.5%6 4.1% (mean 6 SE) inþN trees compared to 32.1% 6

10.5% in controls and 26.9% 6 16.6% inþP trees. There

was a significant relationship between pre- and post-

Frances LAI levels for scrub trees (r2 ¼ 0.59, F1,26 ¼36.58, P , 0.0001), but there were no differences

between pre- and post-Jeanne LAI or between post-

Frances and post-Jeanne LAI. After Hurricane Jeanne,

LAI levels were reduced by 71.2% 6 2.4% in the þNtrees compared to 28.9% 6 12.2% in control trees and

16.2% 6 15.8% in theþP trees. Based on measurements

made over a seven-year period, LAI levels recovered to

pre-hurricane levels by January 2007 for Controls and

þP trees but not until August 2008 forþN trees (Fig. 4).

Subsequent to Aug. 2008, LAI continued to increase for

all nutrient treatments in the scrub zone to exceed pre-

hurricane levels.

In the transition and fringe zones, all nutrient

treatments sustained similar amounts of defoliation that

caused a reduction in LAI by 78.6% 6 1.0%, 80.0% 6

2.6%, and 83.3% 6 2.6% in control, þN, and þP trees,

respectively. The LAI for our experimental trees in the

both of these zones returned to pre-hurricane levels by

January 2007, with no significant differences based on

nutrient treatment (Fig. 4). Additionally, the fringe and

transition trees subsequently experienced large reduc-

tions in LAI in 2008 and in 2010 when there were no

storms, which may have been a result of delayed

mortality in the canopy or persistent drought conditions

in the region during that time period (SFWMD 2009,

Abtew et al. 2010). During these droughts, porewater

salinities increased significantly in all three zones

(repeated-measures ANOVA; F10, 120 ¼ 7.068, P ¼0.000). The scrub zone was consistently hypersaline,

but values fluctuated significantly over time (repeated-

measures ANOVA; F4,44 ¼ 13.2, P , 0.001), with

salinity lowest (47.2 6 4.3 ppt) in April 2005 and highest

(65.4 6 3.9 ppt) in August 2008. Salinity also fluctuated

significantly in the fringe (repeated-measures ANOVA;

F4,44 ¼ 34.8, P , 0.001), with values lowest (28.2 6 3.3

ppt) in October 2004 and the highest (45.2 6 1.1 ppt) in

January 2010. In the transition zone, salinity levels were

intermediate between scrub and fringe level, but also

fluctuated significantly with time (repeated-measures

ANOVA; F4,44 ¼ 21.8, P , 0.001), with values lowest

(39.4 6 1.8 ppt) in October 2004 and the highest (49.6 6

1.1 ppt) in January 2010.

Woody debris.—In April 2005, approximately seven

months after the hurricanes, there was relatively little

downed or standing CWD and FWD in the scrub,

transition, or fringe zones at MI 23 (Table 3). The

woody debris present at that time was primarily in the

sound-wood decay class, which indicated that it had

died recently as a result of the hurricanes (Table 3).

Thus, approximately 60% of the standing dead wood

biomass in the fringe and 80% in the scrub and

transition zones were attributable to the hurricanes.

For the downed wood, approximately 50% of the dead

wood was a direct result of the hurricanes. There was

considerable variability among the plots in the transition

and fringe zones with no significant differences in the

amounts of dead wood in those parts of the mangrove

TABLE 2. Summary of results from the GLM procedure repeated-measures analysis of varianceunivariate tests of hypotheses for within-subject effects performed on leaf area index (LAI)measured over a seven-year period at fertilized Avicennia germinans (scrub and transition zones)and Rhizophora mangle (fringe zone) trees at MI 23.

Source df Type III SS MS F P

Adjusted P

G-G H-F-L

LAI 12 184.05 15.34 281.85 ,0.0001 ,0.0001 ,.0001LAI 3 treatment 24 3.80 0.16 2.91 ,0.0001 0.0006 0.0004LAI 3 zone 24 44.88 1.87 34.36 ,0.0001 ,0.0001 ,.0001LAI 3 treatment 3 zone 48 5.17 0.11 1.98 0.0001 0.0039 0.0026Error (LAI) 852 46.36 0.05G-G 0.5102H-F-L 0.5636

Note: G-G, Greenhouse-Geisser epsilon; H-F-L, Huynh-Feldt-Lecoutre epsilon.


forest. When we resampled the plots two years later in

June 2007, approximately three years after the 2004

hurricanes, there was a large increase in the amount of

recently dead and standing CWD in the fringe zone as a

result of delayed mortality of R. mangle (Fig. 5). In

August 2010, we found a pulse of recently dead R.

mangle twigs and smaller parts of the canopy that had

subsequently fallen to the ground to become part of the

downed FWD in the fringe zone. In addition, delayed

mortality in L. racemosa trees also became evident in

August 2010 and caused a significant increase in the

amount of standing FWD in the transition zone. Unlike

the fringe and transitions zones, the scrub trees suffered

minor losses to the woody portions of their canopies

over the course of our study with no evidence of delayed

mortality.

DISCUSSION

Our results show that, while increasing nutrient

availability enhanced the productivity of scrub man-

groves in the IRL, it also increased their susceptibility to

hurricane damage and decreased their ability to recover

following such disturbances. These findings suggest that

nutrient over-enrichment of the coastal zone may

amplify the impact of hurricanes on mangroves and

lower their resilience to storms and other disturbances

particularly in scrub mangrove forests. In this forest

type, often referred to as dwarf forests, individual trees

are ,1.5 m tall but are relatively old (Lugo and

Snedaker 1974, Lugo 1997). Fertilization experiments

in several such old-growth scrub mangrove stands have

demonstrated that they are nutrient limited and that

addition of the limiting nutrient dramatically increased

their productivity and converted their stunted physiog-

nomy to resemble more vigorously growing trees in

fringing mangrove forests (Feller 1995, Feller et al.

2003a, b, Lovelock et al. 2006, 2009, Martin et al. 2010).

Although the aboveground biomass in scrub mangroves

is low compared to other types of mangrove forests,

these low-stature forests are widespread and have been

documented to dominate much of the mangrove

landscape not only at our study site along the IRL

(Feller et al. 2003b), but also in south Florida (Ross et

al. 2001, 2006, Simard et al. 2006), Belize (Murray et al.

2003, Rodriguez and Feller 2004), Panama (Lovelock et

al. 2005), and throughout the Caribbean (Rivera-

Monroy et al. 2004).

Several studies have observed that their low stature

allows scrub mangroves to escape hurricanes with

negligible defoliation (Craighead 1971, Roth 1992, Lugo

1997, Ross et al. 2006). Experimental studies have

shown that scrub mangroves are extremely sensitive to

increased nutrient availability and respond to nutrient

enrichment with dramatic increases in stature as a result

of increased shoot elongation, branching, and leaf

production (Feller 1995, Feller et al. 2003a, b, 2013,

Lovelock et al. 2004, 2006, Reef et al. 2010), which could

make them more vulnerable to the wind damage

associated with intense tropical storms. Similar to

observations in Australia by Lovelock et al. (2009), the

benefits of increased mangrove biomass in response to

nutrient over-enrichment of the coastal zone will be

offset by lower resilience of mangroves to increased

disturbance.

Despite the potential importance of interactions

between anthropogenic and natural disturbances for

many ecosystems (e.g., Mallin et al. 2002), few

experiments have evaluated the impacts of nutrient

loading on the level of damaged sustained during

disturbance events (Herbert et al. 1999, Lovelock et al.

2011). It is not known how increased nutrients from

anthropogenic sources might affect damage and recov-

ery of mangroves from hurricanes. In a fertilization

experiment in Hawaii, Herbert et al. (1999) found that

experimental nutrient additions had significant effects

on hurricane damage and recovery and that increased

availability of P, the limiting nutrient in a montane

Metrosideros polymorpha forest, resulted in higher

damage and/or decreased resistance coupled with faster

recovery, which indicated an increase in resilience.

TABLE 3. Summary of the biomass of woody debris in the mangrove forest at MI 23 collected inNovember 2005 in 4 3 4 m plots in fringe, transition, and scrub zones (N ¼ 3).

Zone andcanopy position

Sound Intermediate and rotten

FWD (g/m2) CWD (g/m2) FWD (g/m2) CWD (g/m2)

Fringe

Standing 23.0 6 3.1 36.3 6 26.2 1.6 6 0.8 16.6 6 10.8Downed 40.0 6 5.4 42.7 6 14.3 0.1 6 0.0 43.4 6 19.5

Transition

Standing 52.5 6 23.5 167.5 6 115.2 4.2 6 4.1 28.4 6 14.3Downed 39.5 6 5.2 59.4 6 9.1 0.7 6 0.6 136.4 6 98.0

Scrub

Standing 45.2 6 5.6 24.6 6 4.3 1.2 6 1.1 12.9 6 10.7Downed 20.0 6 5.2 3.2 6 1.4 2.3 6 2.0 12.7 6 8.8

Notes: Dead wood on the ground (downed) and in the canopy (standing) was collected andsorted into fine woody debris (FWD) and coarse woody debris (CWD). Samples were categorizedbased on decay class: sound, intermediate, rotten.


Contrary to predictions that resilience and resistance are

inversely related (Hollings 1973, Attiwill 1994), LAI and

growth measurements in our fertilization experiment in

a mangrove forest along the Indian River Lagoon

following hurricanes Frances and Jeanne in September

2004 showed that increased availability of N, the

limiting nutrient at our site, resulted in more structural

damage to the canopy and slower recovery to pre-

hurricane levels. It took four years for the þN trees to

return to pre-hurricane LAI levels compared to two

years for the control trees. These results, which were

only evident in the scrub zone, partially supported our

predictions that the þN trees would sustain more

damage than control trees as a result of decreased

resistance to hurricane winds, but would recover faster

as a result of increased resilience.

For the mangrove forest at MI 23, earlier studies

experimentally identified N as the growth-limiting

nutrient (Feller et al. 2003b, 2013, Lovelock and Feller

2003) and determined that the addition of N fertilizer

(þN) caused a significant increase in plant growth while

the additionþP had no effect on growth. The September

2004 hurricanes resulted in a significant decrease in

growth, measured as shoot elongation, in all zones and

nutrient treatments (Fig. 3). Although the experimental

addition of fertilizer continued, that pattern of decreased

growth persisted over a three-year period following the

hurricanes. This contrasts with other studies that have

found a subsidy effect for mangrove productivity as a

result of increased delivery of nutrients by a storm

(Davis et al. 2004, Lovelock et al. 2011). In contrast to a

similar fertilization experiment in a mangrove forest in

Western Australia, Lovelock et al. (2011) found an

increase in growth in the year following the 2008

Cyclone Pancho, attributed to nutrient and freshwater

subsidies delivered by the storm. However, there was no

canopy damage associated with Cyclone Pancho, but

rather mangroves were exposed to enriched flood

waters.

FIG. 5. Coarse (CWD) and fine (FWD) woody debris from the ground (downed) and from the canopy (standing) in 4 3 4 mplots (N ¼ 3) in the fringe, transition, and zones at MI 23 collected three times over a six-year period.


Although nutrient subsidies enhance primary produc-

tivity of coastal wetlands, nutrient-enrichment experi-

ments have shown that increased nutrients are

detrimental to the long-term maintenance of mangroves

and salt marshes (Verhoeven et al. 2006, Reef et al. 2010,

Deegan et al. 2012). For example, fringing mangroves in

Florida and Belize experienced increased belowground

decomposition, subsidence and loss of habitat stability

in response to nutrient enrichment (Feller et al. 2003b,

McKee et al. 2007). In mangrove fertilization experi-

ments in Australia, nutrient enrichment increased the

sensitivity to hypersalinity and drought in Avicennia

marina trees, which resulted in increased mortality rates

(Lovelock et al. 2009). Several studies found that

competitive interactions, plant-herbivore dynamics,

habitat suitability, and community structure were

altered in response to fertilization (Feller 1995, Lovelock

and Feller 2003, Feller and Chamberlain 2007, Minch-

inton and McKenzie 2008, Feller et al. 2013). Feller et

al. (1999) found that nutrient enrichment dramatically

reduced nutrient use efficiency and the ability of

mangroves to act as a sink for nutrients. In other

coastal wetlands, nutrient enrichment is also widely

recognized as a major driver of habitat loss, eroding

shorelines and reducing carbon storage (e.g., Morris and

Bradley 1999, Cloern 2001, Bertness et al. 2002, 2008,

Turner et al. 2009, Deegan et al. 2012, Turner 2012,

Morris et al. 2013).

Hurricane effects on mangrove canopy.—LAI values

for the þN trees in the scrub zone, which exhibited

vigorous growth in response to the experimental

treatment (Feller et al. 2003b), were reduced ;50% by

Hurricane Frances and another ;25% by Hurricane

Jeanne. Although nutrient availability had no detectable

effect on damage levels in the fringe and transition

zones, the þN trees in the scrub zone sustained higher

PLATE 1. A stand of black and white mangrove trees in Mosquito Impoundment 23 in Avalon State Recreation Area, St. LucieCounty, Florida (USA) on 16 October 2004; three weeks after Hurricane Jeanne and six weeks after Hurricane Frances. The stormsstripped most of the leaves and branches from the mangrove canopy. Photo credit: I. C. Feller.


levels of damage than P-fertilized or control trees. Based

on our repeated measurements of LAI and growth, the

effects of these hurricanes continued to be evident in the

mangroves for at least three to four years after the

passage of these storms.

Results from our study at MI 23 showed that the

damage levels to the mangrove canopy caused by the

September 2004 hurricanes (hurricanes Frances and

Jeanne) along the IRL varied by structural and species

differences among zones and nutrient availability (Fig.

4). Contrary to other studies that found hurricane

damage in coastal forests was similar among mangrove

species and among size classes within species (Odum et

al. 1982, Gresham et al. 1991, Smith et al. 1994), we

found that mangroves of different size classes were

affected differently by hurricanes. Individual plants

(measured repeatedly) changed in LAI over time

differently depending on their zone and nutrient

treatment. In the A. germinans-dominated scrub zone

(Fig. 4), a comparison of before and after LAI values

suggested that these low-stature trees (,2 m tall) in the

interior portions of the mangrove forest sustained very

little defoliation or stem breakage. Similar observations

have been made after other hurricanes (Craighead 1971,

Smith et al. 1994, Lugo 1996, and Ross et al. 2006).

Following each hurricane, layers of wrack lodged in the

tops of scrub trees indicated that they were immersed by

high water during the storms, which likely protected

them from wind damage. In contrast, the taller trees (2–

3 m) in the A. germinans–L. racemosa transition zone,

just seaward of the scrub zone, sustained extensive

defoliation as well as breakage of most of the small

branches out of their canopies. This pattern of damage

further contrasts with the narrow R. mangle-dominated

fringe zone immediately along the water (4–5 m tall),

which experienced less defoliation but more breakage in

the canopy of major branches and boles. Over the course

of our study, recovery to pre-hurricane LAI in the fringe

and transitions zones seemed to be further exacerbated

by a persistent drought in the region.

Although the second of the two storms, Hurricane

Jeanne, was stronger than the first storm, Hurricane

Frances, before and after hurricane comparisons of LAI

at our study site showed that the first storm caused

significantly more damage to the mangrove canopy (Fig.

4). Frances was a category 2 hurricane with maximum

sustained winds of 167 km/h when it made landfall on

South Hutchinson Island on 5 September 2004 (NHC

2004). In contrast, Jeanne was a stronger category 3

hurricane with maximum sustained winds of 195 km/h

when it made landfall three weeks later along the same

portion South Hutchinson Island. It is likely that lower

damage by Hurricane Jeanne was due to less resistance

to the wind as a result of the prior defoliation that had

occurred during Hurricane Frances.

Based on large inputs of woody debris, measured at

three and six years after the September hurricanes, trees

in the fringe and transition zones also experienced

extensive additional damage as a result of delayed

mortality (Fig. 5). When we resampled our plots in 2007,

we found large dead branches in R. mangle trees in the

fringe zone that had been alive in November 2005. By

2010, the evidence of the delayed mortality was detected

in the fringe zone as a pulse of downed FWD, composed

of R. mangle twigs and small stems, and in the transition

zone as a pulse of recently dead standing FWD,

composed mainly small branches in the canopies of L.

racemosa that had died since our 2007 survey.

Krauss et al. (2005) found that the ratio of fine to

coarse woody debris increased with time after the

passage of Hurricane Andrew in south Florida. For

our site along the IRL, we found large increases in the

input of FWD and CWD for more than five years after

the Hurricanes Frances and Jeanne as a result of delayed

mortality in the canopy in the transition and fringe

zones, but with no evidence of delayed mortality in the

scrub zone regardless of nutrient treatment. However,

our data did not reveal any trends in FWD :CWD with

time. Consistent with observations made following

Hurricane Donna (Craighead and Gilbert 1962) and

Hurricane Andrew (e.g., Smith et al. 1994), these results

provide evidence that indirect damage was more severe

than the immediate effects of the storms. Delayed

mortality as an indirect effect of hurricane damage has

also been documented in other ecosystems, including

coral reefs in Jamaica (Knowlton et al. 1981), upland

forests in Puerto Rico (Walker 1995), and forests of the

southeastern United States (Zeng et al. 2009).

Storm recovery

In the year following hurricanes Frances and Jeanne,

the growth rates of both A. germinans and R. mangle

decreased in all three zones. By the second year, growth

rates started to increase but were still lower than they

were before the hurricanes (Feller et al. 2003b). Other

studies have found a similar pattern and have suggested

that pulses of dead wood result in short-term immobi-

lization of nutrients in microbial pools and lead to

decreased forest productivity (Zimmerman et al. 1995,

Scatena et al. 1996, Lugo 2008). Scatena et al. (1996)

showed that it took more than three years for leaf

nutrient concentrations to return to pre-hurricane

concentrations.

Numerous studies have investigated the impact of

hurricanes on coastal ecosystem processes (Greening et

al. 2006). Other researchers have suggested that because

mangrove forests are characterized by low floristic

diversity compared to other tropical and subtropical

forests, the recovery trajectory will be relatively simple

and biological diversity, forest structure, ecosystem

processes, and ecological functions will completely

regain their former states following hurricane distur-

bance (Lugo et al. 1976, Ogden 1992, Smith et al. 1994).

In this study, we found that recovery was not

straightforward, and that nutrient enrichment affected

both the level of impact and the rate of recovery from


hurricane damage in a mangrove forest, with N-enriched

scrub trees taking longer to return to pre-hurricane

conditions than Control trees. Although there is

considerable uncertainty in climate model projections,

the intensity of hurricanes and perhaps the frequency

may increase in the future (Bender et al. 2010, Knutson

et al. 2010, Emanuel 2013, Wang et al. 2014). At the

same time, nutrient loading remains a threat to the

coastal zone and is projected to increase over the next

few decades as fertilizer use increases to meet the

demands of expanding human population (Deegan et

al. 2012). Given that scrub mangrove forests predomi-

nate so much of the mangrove landscape in south

Florida and the Caribbean (e.g., Feller and Mathis 1997,

Lugo 1997, Murray et al. 2004, Rodriguez and Feller

2004, Lovelock et al. 2005, Simard et al. 2006), our

study suggests that the coupling of these anthropogenic

stressors could influence the mechanisms and trajectory

of recovery of mangroves to large-scale disturbances and

thereby diminish their ability to provide valuable

ecosystem services.

ACKNOWLEDGMENTS

We thank the Smithsonian Marine Station in Fort Pierce forlogistical and field support and Anne Chamberlain and R.Feller for countless hours of fieldwork. This research wasfunded by the NASA Climate and Biological Responseprogram (NNX11AO94G) and the NSF MacroSystems Biol-ogy program (EF1065821). This is SMSFP Contribution No.995. We also thank Florida DEP Park Service and St. LucieCounty Mosquito Control and Coastal Management Servicesfor permission to work in Avalon SP.

LITERATURE CITED

Abtew, W., C. Pathak, R. S. Huebner, and V. Ciuca. 2010.Chapter 2: hydrology of the south Florida environment.Pages 1–73 in 2009 South Florida environmental report.Volume I. South Florida Water Management District, WestPalm Beach, Florida, USA.

Attiwill, P. M. 1994. The disturbance of forest ecosystems: theecological basis for conservative management. Forest Ecol-ogy and Management 63:247–300.

Baldwin, A. H., W. J. Platt, K. L. Gathen, J. M. Lessmann, andT. J. Rauch. 1995. Hurricane damage and regeneration infringe mangrove forests of southeast Florida, USA. Journalof Coastal Research 21:169–183.

Ball, M. C. 2002. Interactive effects of salinity and irradianceon growth: implications for mangrove forest structure alongsalinity gradients. Trees 16:126–139.

Bender, M. A., T. R. Knutson, R. E. Tuleya, J. J. Sirutis, G. A.Vecchi, S. T. Garner, and I. M. Held. 2010. Modeled impactsof anthropogenic warming on the frequency of intenseAtlantic hurricanes. Science 327:454–458.

Bertness, M. D., C. M. Crain, C. Holdredge, and N. Sala. 2008.Eutrophication and consumer control of New England saltmarsh primary productivity. Conservation Biology 22:131–139.

Bertness, M. D., P. Ewanchuk, and B. R. Silliman. 2002.Anthropogenic modification of New England salt marshlandscapes. Proceedings of the National Academy of SciencesUSA 99:1395–1398.

Bevan, J. L., II. 2014. Tropical Cyclone Report, HurricaneFrances, 25 August–8 September 2004. National HurricaneCenter, National Weather Service, NOAA, Miami, Florida,USA. http://www.nhc.noaa.gov/data/tcr/AL062004_Frances.pdf

Blake, E. C., E. N. Rappaport, J. D. Jarrell, and C. W. Sandsea.2005. The deadliest, costliest, and most intense United Statestropical cyclones from 1851 to 2004 (and other frequentlyrequested hurricane facts. NOAA Technical MemorandumNWS TPC-4. Tropical Prediction Center, National Hurri-cane Center, Miami, Florida, USA.

Boesch, D. F. 2002. Challenges and opportunities for science inreducing nutrient over-enrichment of coastal ecosystems.Estuaries 25:744–758.

Carlson, P. R., Jr., L. A. Yarbro, K. A. Kaufman, and R. A.Mattson. 2010. Vulnerability and resilience of seagrasses tohurricane and runoff impacts along Florida’s west coast.Hydrobiologia 649:39–53.

Carlson, P. R., L. A. Yarbro, C. F. Zimmermann, and J. R.Montgomery. 1983. Pore water chemistry of an overwashmangrove island. Florida Scientist 46:239–249.

Castaneda-Moya, E., R. R. Twilley, and V. H. Rivera-Monroy.2013. Allocation of biomass and net primary productivity ofmangrove forests along environmental gradients in theFlorida Coastal Everglades, USA. Forest Ecology andManagement 307:226–241.

Cloern, J. E. 2001. Our evolving conceptual model of thecoastal eutrophication problem. Marine Ecology ProgressSeries 210:223–253.

Craighead, F. C. 1971. The trees of south Florida. Volume I.Natural Press, Coral Gables, Florida, USA.

Craighead, F. C., and V. C. Gilbert. 1962. The effects ofHurricane Donna on the vegetation of southern Florida.Quarterly Journal of the Florida Academy of Sciences 25:1–28.

Davis, S. E., III, J. E. Cable, D. L. Childers, C. Coronado-Molina, J. W. Day, Jr., C. D. Hittle, C. J. Madden, E. Reyes,D. Rudnick, and F. Sklar. 2004. Importance of storm eventsin controlling ecosystem structure and function in a Floridagulf coast estuary. Journal of Coastal Research 20:1198–1208.

Deegan, L. A., D. S. Johnson, R. S. Warren, B. J. Peterson,J. W. Fleeger, S. Fagherazzi, and W. M. Wolheim. 2012.Coastal eutrophication as a driver of salt marsh loss. Nature490:388–394.

Dix, N. G., E. J. Phlips, and R. A. Gleeson. 2008. Water qualitychanges in the Guana Tolomato Matanzas National Estua-rine Research Reserve, Florida, associated with four tropicalstorms. Journal of Coastal Research 55:26–37.

Doyle, T. W., and G. F. Girod. 1997. The frequency andintensity of Atlantic hurricanes and their influence on thestructure of south Florida mangrove communities. Pages109–120 in H. F. Diaz and R. S. Pulwarty, editors.Hurricanes: climate and socioeconomic impacts. Springer-Verlag, Heidelberg, Germany.

Emanuel, K. A. 2013. Downscaling CMIP5 climate modelsshows increased tropical cyclone activity over the 21stcentury. Proceedings of the National Academy of SciencesUSA 110:12219–12224.

Feller, I. C. 1995. Effects of nutrient enrichment on growth andherbivory in dwarf red mangrove (Rhizophora mangle).Ecological Monographs 65:477–505.

Feller, I. C., and A. H. Chamberlain. 2007. Herbivore responsesto nutrient enrichment and landscape heterogeneity in amangrove ecosystem. Oecologia 153:607–616.

Feller, I. C., A. H. Chamberlain, C. Piou, S. K. Chapman, andC. E. Lovelock. 2013. Latitudinal patterns of herbivory inmangrove forests: consequences of nutrient over-enrichment.Ecosystems 16:1203–1215.

Feller, I. C., C. E. Lovelock, U. Berger, K. L. McKee, S. B.Joye, and M. C. Ball. 2010. The biocomplexity of mangroveecosystems. Annual Review of Marine Science 2:395–416.

Feller, I. C., and W. N. Mathis. 1997. Primary herbivory bywood-boring insects along a tree-height architectural gradi-ent of Rhizophora mangle L. in Belizean mangrove swamps.Biotropica 29:440–451.


Feller, I. C., K. L. McKee, D. F. Whigham, and J. P. O’Neill.2003a. Nitrogen vs. phosphorus limitation across andecotonal gradient in a mangrove forest. Biogeochemistry62:145–175.

Feller, I. C., D. F. Whigham, K. L. McKee, and C. E.Lovelock. 2003b. Nitrogen limitation of growth and nutrientdynamics in a disturbed mangrove forest, Indian RiverLagoon, Florida. Oecologia 134:405–414.

Feller, I. C., D. F. Whigham, J. P. O’Neill, and K. M. McKee.1999. Effects of nutrient enrichment on within-stand nutrientcycling in mangrove ecosystems in Belize. Ecology 80:2193–2205.

Greening, H., P. Doering, and C. Corbett. 2006. Hurricaneimpacts on coastal ecosystems. Estuaries and Coasts 29:877–879.

Gresham, C. A., T. M. Williams, and D. J. Lipscomb. 1991.Hurricane Hugo wind damage to southeastern U.S. coastalforest tree species. Biotropica 23:420–426.

Herbert, D. A., J. H. Fownes, and P. M. Vitousek. 1999.Hurricane damage to a Hawaiian forest: nutrient supply rateaffects resistance and resilience. Ecology 80:908–920.

Hollings, C. S. 1973. Resilience and stability of ecologicalsystems. Annual Review of Ecology and Systematics 4:1–23.

Imbert, D., P. Labbe, and A. Rousteau. 1996. Hurricanedamage and forest structure in Guadeloupe, French WestIndies. Journal of Tropical Ecology 12:663–680.

Jiang, J., D. L. DeAngelis, G. H. Anderson, and T. J. Smith III.2014. Analysis and simulation of propagule dispersal andsalinity intrusion from storm surge on the movement of amarsh–mangrove ecotone in South Florida. Estuaries andCoasts 37:24–35.

Knowlton, N., J. C. Lang, M. C. Rooney, and P. Clifford. 1981.Evidence for delayed mortality in hurricane-damaged Jamai-can staghorn corals. Nature 294:251–252.

Knutson, T. R., J. L. McBride, J. Chan, K. Emanuel, G.Holland, C. Landsea, I. Held, J. P. Kossin, A. K. Srivastava,and M. Sugi. 2010. Tropical cyclones and climate change.Nature Geoscience 3:157–163.

Krauss, K. W., R. R. Twilley, T. J. Smith III, K. R. T. Whelan,and J. K. Sullivan. 2005. Woody debris in the mangroveforests of South Florida. Biotropica 37:9–15.

Lapointe, B. E., B. J. Bedford, and R. Baumberger. 2006.Hurricanes Frances and Jeanne remove blooms of theinvasive green alga Caulerpa brachypus forma parvifolia(Harvey) Cribb from coral reefs off northern Palm BeachCounty, Florida. Estuaries and Coasts 29:966–971.

Liu, K. 2007. Uncovering prehistoric hurricane activity.American Scientist 95:126–133.

Lovelock, C. E., M. C. Ball, B. Choat, B. M. J. Engelbrecht,N. M. Holbrook, and I. C. Feller. 2006. Linking physiolog-ical processes with mangrove forest structure: phosphorusdeficiency limits canopy development, hydraulic conductivityand photosynthetic carbon gain in dwarf Rhizophora mangle.Plant, Cell and Environment 29:793–802.

Lovelock, C. E., M. C. Ball, K. Martin, and I. C. Feller. 2009.Nutrient enrichment increases mortality of mangroves. PLoSONE 4:e5600.

Lovelock, C. E., and I. C. Feller. 2003. Photosyntheticperformance and resource utilization of two mangrovespecies coexisting in hypersaline scrub forest. Oecologia134:455–462.

Lovelock, C. E., I. C. Feller, M. F. A. Adame, R. R. Reef,H. M. Penrose, L. Wei, and M. C. Ball. 2011. Intense stormsand the delivery of materials that relieve nutrient limitationsin mangroves of an arid zone estuary. Functional PlantBiology 38:514–522.

Lovelock, C. E., I. C. Feller, K. L. McKee, B. M. J.Engelbrecht, and M. C. Ball. 2004. The effect of nutrientenrichment on growth, photosynthesis and hydraulic con-ductance of dwarf mangroves in Panama. FunctionalEcology 18:25–33.

Lovelock, C. E., I. C. Feller, K. L. McKee, and R. Thompson.2005. Variation in mangrove forest structure and sedimentcharacteristics in Bocas del Toro, Panama. CaribbeanJournal of Science 41:456–464.

Lugo, A. E. 1996. Caribbean island landscapes: indicators ofthe effects of economic growth on the region. Environmentand Development Economics 1:128–136.

Lugo, A. E. 1997. Old-growth mangrove forests in the UnitedStates. Conservation Biology 11:11–20.

Lugo, A. E. 2008. Visible and invisible effects of hurricanes onforest ecosystems: an international review. Austral Ecology33:368–398.

Lugo, A. E., M. Sell, and S. C. Snedaker. 1976. Mangroveecosystem analysis. Pages 113–145 in B. C. Patten, editor.Systems analysis and simulation in ecology 4. AcademicPress, New York, New York, USA.

Lugo, A. E., and S. C. Snedaker. 1974. The ecology ofmangroves. Annual Review of Ecology and Systematics 5:39–64.

Mallin, M. A., M. H. Posey, M. R. McIver, D. C. Parson, S. H.Ensign, and T. D. Alphin. 2002. Impacts and recovery frommultiple hurricanes in a piedmont-coastal plain river system.BioScience 52:999–1010.

Martin, K. C., D. Bruhn, C. E. Lovelock, I. C. Feller, J. R.Evans, and M. C. Ball. 2010. Nitrogen fertilization enhanceswater use efficiency in a saline environment. Plant, Cell andEnvironment 33:344–357.

McCoy, E. D., H. R. Mushinsky, D. Johnson, and W. E.Meshaka, Jr. 1996. Mangrove damage caused by HurricaneAndrew on the southwestern coast of Florida. Bulletin ofMarine Science 59:1–8.

McKee, K. L., D. Cahoon, and I. C. Feller. 2007. Caribbeanmangroves adjust to rising sea-level through biotic controlson soil elevation change. Global Ecology and Biogeography16:546–556.

Milbrandt, E. C., J. M. Greenawalt-Boswell, P. D. Sokoloff,and S. A. Bortone. 2006. Impact and response of southwestFlorida mangroves to the 2004 hurricane season. Estuariesand Coasts 29:979–984.

Minchinton, T. E., and L. A. McKenzie. 2008. Nutrientenrichment affects recruitment of oysters and barnacles in amangrove forest. Marine Ecology Progress Series 354:181–189.

Morris, J. T., and P. M. Bradley. 1999. Effects of nutrientloading on the preservation of organic carbon in wetlandsediments. Limnology and Oceanography 44:699–702.

Morris, J. T., G. P. Shaffer, and J. A. Nyman. 2013. BrinsonReview: perspectives on the influence of nutrients on thesustainability of coastal wetlands. Wetlands 33:975–988.

Murray, M. R., S. A. Zisman, P. A. Furley, D. M. Munro, J.Gibson, J. Ratter, S. Bridgewater, C. D. Minty, and C. J.Place. 2003. The mangroves of Belize: Part 1. Distribution,composition and classification. Forest Ecology and Manage-ment 174:265–279.

NHC. 2004. 2004 tropical cyclone advisory archive. NationalHurricane Center, National Weather Service, NOAA,Miami, Florida, USA. http://www.nhc.noaa.gov/archive/2004/

NHC. 2012. The Saffir-Simpson hurricane wind scale. NationalHurricane Center, National Weather Service, NOAA,Miami, Florida, USA. http://www.nhc.noaa.gov/pdf/sshws.pdf

Odum, W. E., C. C. McIvor, and T. J. Smith III. 1982. Theecology of the mangroves of South Florida: a communityprofile. FWS/OBS—81/24. U.S. Fish and Wildlife Service,Office of Biological Services, Washington, D.C., USA.

Ogden, J. C. 1992. The impact of Hurricane Andrew on theecosystems of south Florida. Conservation Biology 6:488–490.

Paperno, R. D., M. Tremain, D. H. Adams, A. P. Sebastian,J. T. Sauer, and J. Dutka-Gianelli. 2006. The disruption andrecovery of fish communities in the Indian River Lagoon,


Florida, following two hurricanes in 2004. Estuaries andCoasts 29:1004–1010.

Piou, C., I. C. Feller, U. Berger, and F. Chi. 2006. Zonationpatterns of Belizean offshore mangrove forests 41 years aftera catastrophic hurricane. Biotropica 38:365–374.

Proffitt, C. E., E. C. Milbrandt, and S. E. Travis. 2006. Redmangrove (Rhizophora mangle) reproduction and seedlingcolonization after Hurricane Charley: comparisons of Char-lotte Harbor and Tampa Bay. Estuaries and Coasts 29:972–978.

R Core Team. 2009. R: a language and environment for statisticalcomputing. R Foundation for Statistical Computing, Vienna,Austria. http://www.R-project.org/

Reef, R., I. C. Feller, and C. E. Lovelock. 2010. Nutrition ofmangroves. Tree Physiology http://dx.doi.org/10.1093/treephys/tpq048

Rey, J., and T. Kain. 1991. A guide to the salt marshimpoundments of Florida. University of Florida, FloridaMedical Entomology Laboratory, Vero Beach, Florida,USA.

Rey, J. R., R. A. Crossman, T. R. Kain, and D. S. Taylor. 1986.An overview of impounded mangrove forests along asubtropical lagoon in east-central Florida, USA. Pages341–350 in L. J. Bhosale, editor. Proceedings of NationalSymposium on Biology, Utilization and Conservation ofMangroves, 18–20 November 1985. Shivaji University,Kolhapur, India.

Rey, J. R., J. Shaffer, R. Crossman, and D. Tremain. 1990.Above-ground primary production in impounded, ditched,and natural Batis-Salicornia marshes along the Indian RiverLagoon, Florida, USA. Wetlands 10:151–171.

Rey, J. R., J. Shaffer, T. Kain, R. Stahl, and R. Crossman.1992. Sulfide variation in the pore and surface waters ofartificial salt-marsh ditches and a natural tidal creek.Estuaries 15:257–269.

Ridler, M. S., R. C. Dent, and D. A. Arrington. 2006. Effects oftwo hurricanes on Syringodium filiforme, manatee grass,within the Loxahatchee River Estuary, Southeast Florida.Estuaries and Coasts 29:1019–1025.

Rivera-Monroy, V. H., et al. 2004. A biogeochemical concep-tual framework to develop long term ecological research andsustain coastal management in the wider Caribbean Region.BioScience 54:843–856.

Rodriguez, W., and I. C. Feller. 2004. Mangrove landscapecharacterization and change in Twin Cays, Belize using aerialphotography and IKONOS satellite data. Atoll ResearchBulletin 513:1–22.

Ross, M. S., P. L. Ruiz, J. P. Sah, D. L. Reed, J. Walters, andJ. F. Meeder. 2006. Early post-hurricane stand developmentin fringe mangrove forests of contrasting productivity. PlantEcology 185:283–297.

Ross, M. S., P. L. Ruiz, G. J. Telesnicki, and J. F. Meeder.2001. Estimating above-ground biomass and production inmangrove communities of Biscayne National Park, Florida(U.S.A.). Wetlands Ecology and Management 9:27–37.

Roth, L. C. 1992. Hurricanes and mangrove regeneration:effects of Hurricane Joan, October 1988, on the vegetation ofIsla del Veneto, Bluefields, Nicaragua. Biotropica 24:375–384.

Sallenger, A. H., H. F. Stockdon, L. Fauver, M. Hansen, D.Thompson, C. W. Wright, and J. Lillycrop. 2006. Hurricanes2004: an overview of their characteristics and coastal change.Estuaries and Coasts 29:880–888.

Scatena, F. N., S. Moya, C. Estrada, and J. D. Chinea. 1996.The first five years of reorganization of aboveground biomassand nutrient use following Hurricane Hugo in the Bisleyexperimental watersheds, Luquillo Experimental Forest,Puerto Rico. Biotropica 28:424–440.

SFWMD. 2009. South Florida Water Management District,Media Advisory for March 10, 2009. http://sfwmd.gov/portal/page/portal/xrepository/sfwmd_repository_pdf/ma_2009_0310_drought_ebriefing.pdf

Sherman, R. E., T. J. Fahey, and P. Martinez. 2001. Hurricaneimpacts on a mangrove forest in the Dominican Republic:damage patterns and early recovery. Biotropica 33:393–408.

Silver, W. L., S. Brown, and A. E. Lugo. 1996. Effects ofchanges in biodiversity on ecosystem function in tropicalforests. Conservation Biology 10:17–24.

Simard, M., K. Zhang, V. H. Rivera-Monroy, M. S. Ross, P. L.Ruiz, E. Castaneda-Moya, R. R. Twilley, and E. Rodriguez.2006. Mapping height and biomass of mangrove forests inEverglades National Park with SRTM elevation data.Photogrammetric Engineering and Remote Sensing 72:299–311.

Smith, T. J., III, G. H. Anderson, K. Balentine, G. Tiling, G. A.Ward, and K. R. T. Whelan. 2009. Cumulative impacts ofhurricanes on Florida mangrove ecosystems: sedimentdeposition, storm surges and vegetation. Wetlands 29:24–34.

Smith, T. J., III, M. B. Robblee, H. R. Wanless, and T. W.Doyle. 1994. Mangroves, hurricanes, and lightning strikes.BioScience 44:256–262.

Steward, J. S., R. W. Virnstein, M. A. Lasi, L. J. Morris, J. D.Miller, L. M. Hall, and W. A. Tweedale. 2006. The impactsof the 2004 hurricanes on hydrology, water quality, andseagrass in the central Indian River Lagoon. Estuaries andCoasts 29:954–965.

Systat. 2004. Systat 11. Systat Software, San Jose, California,USA.

Tomasko, D. A., C. Anastasiou, and C. Kovach. 2006.Dissolved oxygen dynamics in Charlotte Harbor and itscontributing watershed, in response to Hurricanes Charley,Frances, and Jeanne—impacts and recovery. Estuaries andCoasts 29:932–938.

Turner, R. E. 2012. Beneath the salt marsh canopy: loss of soilstrength with increasing nutrient loads. Estuaries and Coasts34:1084–1093.

Turner, R. E., B. L. Howes, J. M. Teal, C. S. Milan, E. M.Swenson, and D. D. Goehringer-Toner. 2009. Salt marshesand eutrophication: an unsustainable outcome. Limnologyand Oceanography 54:1634–1642.

Verhoeven, J. T. A., B. Arheimer, C. Yin, and M. M. Hefting.2006. Regional and global concerns over wetlands and waterquality. Trends in Ecology and Evolution 21:96–103.

Vogt, J., A. Skora, I. C. Feller, C. Piou, G. Coldren, and U.Berger. 2011. Investigating the role of impoundment andforest structure on the resistance and resilience of mangroveforests to hurricanes. Aquatic Botany 97:24–29.

Walker, L. R. 1995. Timing of post-hurricane tree mortality inPuerto Rico. Journal of Tropical Ecology 11:315–320.

Wang, H., et al. 2014. How well do global climate modelssimulate the variability of Atlantic tropical cyclones associ-ated with ENSO? Journal of Climate 27:5673–5692.

Wang, P., and M. H. Horwitz. 2007. Erosional and depositionalcharacteristics of regional overwash deposits caused bymultiple hurricanes. Sedimentology 54:545–564.

Zeng, H., J. Q. Chambers, R. I. Negron-Juarez, G. C. Hurtt,D. B. Baker, and M. D. Powell. 2009. Impacts of tropicalcyclones on U.S. forest tree mortality and carbon flux from1851 to 2000. Proceedings of the National Academy ofSciences USA 106:7888–7892.

Zimmerman, J. K., W. M. Pulliam, D. J. Lodge, V. Quinones-Orfila, N. Fetcher, S. Guzman-Grajales, J. A. Parrotta, C. E.Asbury, L. R. Walker, and R. B. Waide. 1995. Nitrogenimmobilization by decomposing woody debris and therecovery of tropical wet forest from hurricane damage. Oikos72:314–322.


Documents

Nutrient enrichment intensiﬁes hurricane impact in scrub ...376158/UQ376158_fulltext.p… · 2006, Ridler et al. 2006, Sallenger et al. 2006, Steward et al. 2006, Tomasko et al