Ocean & Coastal Management 110 (2015) 38e45

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Ocean & Coastal Management

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Restoration versus natural regeneration in a neotropical mangrove:

Effects on plant biomass and crab communities
Alexander C. Ferreira*, 1, Gislene Ganade, Jose

Luiz de Attayde
Departamento de Ecologia, Centro de Bioci^
encias, Universidade Federal do Rio Grande do Norte, Campus Lagoa Nova, Natal, RN CEP: 59161175, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Mangrove restoration is a powerful tool for reconstructing degraded tropical estuaries worldwide. The
Received 19 December 2014 level of intervention necessary for rebuilding a mangrove area is still under study because this system is
Received in revised form quite dynamic and some degraded areas are able to recover by themselves. We compared a Restored Area
15 March 2015
planted with Rhizophora mangle and a Self-recovered Area, to investigate how they would differ in
Accepted 21 March 2015
respect to their plant and crab assemblages. In each area, 10 plots were randomly sampled for measuring
Available online
tree richness, density, diameter at breast height and biomass, as well as crab richness and density after
five years from recover. Plant height and biomass, as well as crab density, were significantly higher in the
Keywords:
Biomass production
Restored in relation to the Self-recovered Area. However, tree richness was higher in the Self-recovered
Crab richness Area and crab assemblage reached in five years a similar composition in assisted, naturally recovered and
Functional group natural areas, showing the high resilience of this important functional group. Active planting of R. mangle
Goniopsis cruentata propagules can significantly improve mangrove recovery in sites with high propagule predation,
Mangrove restoration increasing tree biomass and accelerating the return of animal functional groups such as crabs. However,
Wetland management if resources for active restoration are scarce, passive recovery can be a successful low cost alternative for
mangrove restoration that preserves tree diversity and crab assemblages.
© 2015 Elsevier Ltd. All rights reserved.

1. Introduction 2010; Walters, 2000).

Mangroves are highly productive biological communities that
occupy around 15
106 km2 of tropical and subtropical coasts
worldwide (FAO, 2007; Lacerda, 2002). At least 35% of mangrove
forests have been destroyed in the past decades by human settle-
ments, wood extraction and shrimp culture (Valiela et al., 2001)
leaving many deforested and abandoned areas in need of restora-
tion (Alongi, 2002). However, to restore a degraded ecosystem to a
pristine condition is not an easy task, because most ecosystems are
in permanent change, and estuarine mangroves are a good example
(Alongi, 2009; Wyant et al., 1995). On the other hand, the effec-
tiveness of mangrove restoration programs to significantly improve
ecosystem function has been doubted, due to the use of only one or
few tree species, a low richness when compared to natural areas
(Ellison, 2000; Lewis III, 2005; Rovai et al., 2012; Salmo III and Duke,
* Corresponding author.
E-mail addresses: alexcrab90@hotmail.com (A.C. Ferreira), gganade@gmail.com
(G. Ganade), cocattayde@gmail.com (J. Luiz de Attayde).
1 ^ncias do Mar (LABOMAR), Universidade Federal
Present address: Instituto de Cie
do Ceara
, Avda da Aboliça~o 3207, Meireles, Fortaleza, CE, CEP: 60165 081, Brazil.
Tree development is an important and commonly measured
feature of a restored ecosystem, because key ecosystem functions
and faunal colonization are dependent on vegetation structure,
biomass and diversity. Planted mangroves can reach high tree
development in height, diameter or biomass (Hong, 1996; Ferreira
et al., 2007; Macintosh et al., 2002), but Ross et al. (2001) found that
naturally recovered Neotropical mangroves have achieved similar
tree development than planted ones. Choosing a better cost/benefit
management procedure in such forests is impaired by scarcity on
studies comparing equal lifetime planted and naturally recovered
areas. Studied natural stands used to compare with planted were of
unknown age or older (Bernini et al., 2013; Martinuzzi et al., 2009;
Shafer and Roberts, 2008). Alternatively, the return of faunal
functional groups can be an indicator of forest restoration success
(Babin-Fenske and Anand, 2010; Gibb and Cunningham, 2013;
Gollan et al., 2011; Jansen, 1997). In mangrove forests some
studies show evidences that important invertebrate groups like
Brachyuran crabs may be more diverse in planted stands despite
restoration being implemented with only one or few tree species
(Al-Khayat and Jones, 1999; Ashton et al., 2003; Bosire et al., 2004,
2008; Macintosh et al., 2002).

http://dx.doi.org/10.1016/j.ocecoaman.2015.03.006
0964-5691/© 2015 Elsevier Ltd. All rights reserved.
 A.C. Ferreira et al. / Ocean & Coastal Management 110 (2015) 38e45
Crabs of the families Ocypodoidea and Grapsoidea (Brachyura;
Decapoda) (Ng et al., 2008) are among the most abundant and
ecologically significant mangrove dweller animals. They are
‘ecosystem engineers’ that play important roles on sediment
topography and biogeochemistry, vegetation structure and primary
production (Jones et al., 1994; Kristensen, 2008; Lee, 2008;
Robertson and Daniel, 1989; Warren and Underwood, 1986).
Despite their role in affecting overall community structure and
ability to serve as important indicators of natural and managed
forests conservation status (Ashton et al., 2003; Bosire et al., 2004;
Macintosh et al., 2002; Ruwa, 1997), their effects have been rarely
assessed in neotropical mangroves (but see Ferreira et al., 2007,
2013). Therefore, the relationship between mangrove develop-
ment and crab assemblage is a relevant aspect that needs evalua-
tion in mangrove restoration programs. Several studies designed
allometric equations for calculate mangroves biomass (see Review
of Komiyama et al., 2008), while others compared carcinofauna
between natural and reforested stands (see Review of Bosire et al.,
2008), but there are not studies comparing both carcinofauna and
tree biomass differences between these forests types.
The aim of this study was to compare tree and crab diversities
and community structure of two mangrove deforested areas of the
same age, one planted with propagules of red mangrove, Rhizo-
phora mangle, and the other naturally recovered. Here, we tested
the hypothesis that the two areas neither differ significantly in
plant richness and biomass nor differ in crab richness or density. A
rejection or acceptance of this hypothesis would provide evidence
for or against the effectiveness of R. mangle monospecific planting
for neotropical mangrove restorations.
2. Materials and methods
2.1. Study area
The study was performed in a mangrove area in Jaguaribe River
(35140 0600 W/5 450 4200 S), tributary of the Potengi River in Natal,
Rio Grande do Norte, Brazil (Fig. 1A). The climate is tropical, with air
temperatures between 20 and 31  C and total precipitation around
1900 mm. The Potengi River is a temporary river (rainy season
MarcheJuly) with a catchment drainage of 3180 km2 (Silva et al.,
2007) receiving wastewaters from Natal and other smaller towns
throughout the year. The estuary is covered by 15.61 km2 of
Fig. 1. Study area at Potengi estuary, northeast Brazil. A. Shaded areas indicate mangroves in Potengi River estuary. B. Satellite image of studied areas in Jaguaribe River. Arrows
show the restored and self recovered experimental areas deforested, before experiment starting. Asterisks (*) show small creeks formed laterally to constructed dams. Areas are
surrounded by native mangroves.
39
mangrove forests (Maia et al., 2005) dominated by the red
mangrove R. mangle L., but white mangrove Laguncularia racemosa
Gaertn. and black mangrove Avicennia schaueriana Stapf. & Leech.
also occur in lower abundance (Ferreira and Sankarankutty, 2002).
Many mangrove areas have been cleared for intensive exotic
shrimp culture (Penaeus vannamei), but this economic activity has
decreased in recent years. Shrimp ponds are constructed enclosing
a mangrove area with dams (aprox. 2 m height) constructed with
mangrove wood and mud; trees are chopped and retired, and
chemical products added to increase soil pH to levels compatible
with shrimp development. Surveying the river we found an area
cleared in 2003 but abandoned before ponds were completely
implemented (Fig. 1B). This experimental area encompasses a
mosaic of preserved mangrove, shrimp ponds and secondary ri-
parian forest. Partially constructed dams did not impaired hydro-
logic features of area, which receives brackish water from high
intertidal fringe and experiences semidiurnal tides. However, dur-
ing the tree clearing the soil was physically altered and populations
of crabs greatly affected. The area was originally dominated by
R. mangle, with far lower abundance of L. racemosa. In spite of high
numbers of R. mangle and L. racemosa propagules being brought by
tides from surrounding mangroves, only very sparse (<0.004 in-
dividuals m2, when 3.2 individuals m2 in mature forest - Silva
et al., 2007) seedlings and small trees (0.3e0.7 m height) were
established naturally 3 years after deforestation, by the time the
experiment started.
2.2. Experimental design and parameters measures
The study area encompasses two adjacent areas (Fig. 1B) both
deforested 3 years before the experiment started, so collection of
any data on soil structure and tree development before deforesta-
tion was not possible. However, neighbor native forest was used as
reference (Fig. 1B). Unfortunately, no area available for replication
was found at the start of the experiment. Large scale experiments
are sometimes hard to replicate decreasing power of conclusions,
but they may be more realistic than experiments performed at
lower scales, a trade-off imposed by costs and scarcity on experi-
mental ecosystems (Carpenter, 1989; Hurlbert, 1984). Additionally,
peculiarities of the mangrove ecosystem and features of the studied
areas imposed methodological limitations for dividing areas in
more than one experimental unit without suffering from treatment
40 A.C. Ferreira et al. / Ocean & Coastal Management 110 (2015) 38e45
contamination; therefore, the area was restored entirely through
planting.
Before planting, sediment of both smaller and larger areas was
characterized by sampling 10 plots of 5
5 m (Schaeffer-Novelli
and Cintro
n, 1986) selected at random out of 100 equally spaced
plots defined as a grid over a satellite image. Analysis of sediment
texture was performed at the Laboratory using the Gravimetric
Method (Machado, 2002). Salinity was measured in water samples
extracted 15 cm deep in soil, using an Optical Refractometer
(Schaeffer-Novelli and Cintro
n, 1986). We measured soil penetra-
bility (i.e. substrate softness) by releasing vertically a centimeter
graduated steel rod of 45 cm length, 1.3 cm diameter and 370 g
weight, from a height of 1.2 m (Ferreira et al., 2013). “Restored Area”
(Fig. 1B) was reforested in the rainy season of 2006 by planting
propagules of R. mangle free from herbivore damage and approxi-
mately 25 cm long. A total of 27,740 propagules were collected at
river coasts and planted at higher densities (4.14 individuals m2)
than natural mangroves to counteract crab predation (Ferreira
et al., 2007). Propagules were buried 5e8 cm in mud, every 0.5 m
in parallel transects 0.5 m apart. In the other area, or “Self-recov-
ered” (Fig. 1B), trunks of cut down trees were removed by shrimp
breeders after clearing, and no further manipulation was made,
maintaining the area to natural colonization. Soil features were
measured in the native neighbor forest in 2009.
Five years after planting, trees were measured in both areas in
10 quadrats of 5
5 m (Schaeffer-Novelli and Cintro
n, 1986)
randomly selected using the same methodology described above.
All trees were counted. Trees higher than 1.8 m (hereafter called
“mature” because propagule production initiated around this
average size) had their diameter at breast height (dbh) and height
(H) measured. Trees lower than 1.8 m (“young”) were for conve-
nience considered post planting self-recruits. Density (trees/m2) of
both size categories was calculated. Height and dbh of some dwarf
mature trees (<1.8 m), recognizable by their lower height/dbh
relation and smaller leaves than young trees (Cintro
n and
Schaeffer-Novelli, 1983) were included in the mature tree data-
base. Aboveground biomass was calculated using an allometric
equation constructed by measuring weight, height and dbh of 20
mature trees of R. mangle and L. racemosa. The allometric equations
that best fitted the data were polynomial and included dbh only.
For R. mangle trees, biomass in grams was equal to 427.26(dbh2)e
544.45(dbh)þ994.63, and for L. racemosa biomass was equal to
299.43(dbh2)e486.06(dbh)þ393.04 with R2 coefficient of 0.85 and
0.99 respectively. At natural adjacent areas only the average tree
density was measured, obtaining a similar value (around 3.2 in-
dividuals m2) of a nearly natural area studied by Silva et al. (2007)
with same R. mangle predominance, so this latter study was used as
reference of biomass production of native mangrove.
Burrowing crabs of Grapsidae and Sesarmidae (Grapsoidea) as
well as Ocypodidae and Ucididae (Ocypodoidea) families occur in
the Potengi mangroves (Ferreira and Sankarankutty, 2002). Mid-
littoral crabs species have been surveyed extensively in sediment,
tree canopies and roots in the study areas since 2004. The ecolog-
ically significant and abundant Grapsid Goniopsis cruentata
(Ferreira et al., 2013), is a medium sized (5.0 cm carapace width e
c.w.) mobile and non-burrowing crab (Warner, 1969) very abun-
dant under mangroves at adjacent areas. It is a significant propa-
gule consumer under canopy and their vicinities (Ferreira et al.,
2007, 2013). Ucides cordatus is a large litter consumer neotropical
burrowing crab. Density of G. cruentata individuals 2.5 cm c.w.
and U. cordatus (4.5 cm c.w.) (sub-adults and adults) was esti-
mated by counting individuals before and after 5 years from the
beginning of the experiment in 10 randomized quadrats of 5
5 m.
G. cruentata was counted visually (Ferreira et al., 2013). Density of
U. cordatus and fiddler crabs Uca spp. was estimated by counting
burrows inside the quadrats described above. Higher density of
these Ocypodoids is associated to more soil turn-over. Counts were
expressed as burrows m2 which is equivalent to individuals m2
(Branco, 1993; Skov and Hartnoll, 2001). U. cordatus’ burrows
<2.5 cm diameter were considered juveniles (carapace < 4 cm in
width e Carmona-Suarez and Guerra-Castro, 2012) and not coun-
ted. Dense prop roots coverage in Restored Area, and substrate
coverage by Bostrychia sp. (Rodophyta) in Self-recovered impaired
counts of burrows of Uca spp. populations at 5 year after planting.
Crab counting in native neighbor areas was performed in 2009.
2.3. Statistical analysis
For compare salinity and penetrability measures, albeit
comparing two groups (areas) we preferred ANOVA over t-test. A
PERMANOVA analysis using BrayeCurtis tests in 9999 random
permutations (Anderson, 2001) was run to compare number of
young, number of mature, dbh, height and biomass between trees
of Restored and Self-recovered Areas. An ANOVA was also used to
compare G. cruentata and U. cordatus crabs densities between the
two managed areas before the beginning of the experiment (2006)
and five years after planting (2011). Analyses were run using
respectively “R” and Systat softwares.
3. Results
Penetrability was significantly different between the two areas
but not salinity (ANOVA respectively F1,18 ¼ 7.7; p < 0.05 and
F1,13 ¼ 0.005; p > 0.05) (Table 1) at starting. R. mangle was the only
tree recorded in the Restored Area plots. In the Self-recovered Area,
L. racemosa was also present and was more abundant than
R. mangle. There was higher seedling regeneration in the Self-
recovered Area, where seedlings of L. racemosa were observed in
seven out of ten plots surveyed, while seedlings of R. mangle were
recorded in only four of these plots.
PERMANOVA analysis revealed a significant difference between
Restored and Self-recovered Areas for tree variables (F1,18 ¼ 17.88;
p < 0.001). After five years of restoration, the Restored Area had
higher mature tree densities (Fig. 2A) but lower young tree density
(Fig. 2B) than the Self-recovered Area, despite not significant dif-
ferences in average dbh (Fig. 2C). Additionally, mean tree height
(Fig. 2D) and total tree biomass (Fig. 2E and F) were higher in the
Restored Area.
G. cruentata density was always higher in the Restored than in
the Self-recovered Area (F1,36 ¼ 4.6; p < 0.05; Fig. 3A), but
U. cordatus density was similar between the two areas (Fig. 3B,
Table 1); both species were less abundant than in native areas.
G. cruentata density increased faster over time than U. cordatus
density five years after planting (F1,36 ¼ 4.3 p < 0.05; Fig. 3).
Grapsoid richness in Restored Area was the same of native forest at
the start and before planting experiment. Self-recovered Area
showed the same Grapsoid species set 5 years after the start of the
experiment with the exception of Armases angustipes. Ocypodoids
reached the same richness of native forests in both areas only 5
years after the start of the experiment (Table 2).
4. Discussion
A major goal of ecological restoration is to achieve the recovery
of biodiversity and its role in ecosystem functioning and services
(Holl and Aide, 2011; SER, 2004). Depending on the frequency and
intensity of disturbances (Biswas et al., 2012; Jones and Schmitz,
2009), some ecosystems may need human assistance for active
restoration, in order to improve or accelerate the return of their
ecological functions and self-sustainability (SER, 2004). Many
 A.C. Ferreira et al. / Ocean & Coastal Management 110 (2015) 38e45 41

Table 1
Sediment parameters measured at the two study sites previous to planting. Uca burrows are expressed as burrows/m2; number of G. cruentata and U. cordatus are expressed as
before/after planting as individuals/m2. Values of Penetrability and Salinity are means ± SD. Both areas were cleared in 2003. Data from native areas are from 2009.

Forest Size (ha) Penetrability (cm) Salinity (%o) % Clay þ Silt Uca species burrow density G. cruentata U. cordatus

Restored 0.67 14.23 ± 2.11 17.2 ± 2.58 Silty sand U. (Leptuca) cumulanta y 300 0.1/0.32 0.0/0.07
Self Recovered 2.30 10.67 ± 3.36 16.7 ± 15.86 Silty sand to sand U. (Leptuca) cumulanta, > U. (Minuca) rapax y 80e100 0.0/0.15 0.0/0.05
Native e 16.20 ± 3.40 16.20 ± 3.60 Silty sand U. (Leptuca) cumulanta, < Uca (Minuca) thayeri y 100 2.2 ± 0.3 4.0 ± 1.0

Fig. 2. Mangrove trees developing in Restored and Self Recovered mangrove areas in northeast Brazil 5 years after restoration (PERMANOVA F1,18 ¼ 17.88; p < 0.001). Post-hoc test
results are in graphics (NSe not significant). Juvenile (A) and mature (B) tree density; mean dbh (C) and mean height (D). Total mature tree biomass for Rhizophora mangle and
Laguncularia racemosa in Restored and Self-recovered mangroves was calculated using our own allometric equation (E) and the equation of Medeiros and Sampaio (2008) (F). Error
bars represent standard error of mean. Scales on vertical axis were adapted to maintain axis size in E and F.

Fig. 3. Changes in density (individuals/m2) of Goniopsis cruentata and Ucides cordatus before and five years after restoration. Black lines, Restored Area; gray lines, Self-recovered
Area.
42 A.C. Ferreira et al. / Ocean & Coastal Management 110 (2015) 38e45
Table 2
Size and occurrence of Brachyuran crab species of Superfamilies Grapsoidea and Ocypodoidea found in restored and self recovered areas before (2006) and after 5 years (2011)
of mangrove restoration. Crab size: S-small; M-medium; L-large. Occurrence information is represented by: –, absence; þ, juveniles; þþ, juveniles to adults.
Species Restored
Size Before
Grapsoids
Goniopsis cruentata M þþ
Pachygrapsus gracilis S þþ
Sesarma rectum S þ
Sesarma curacaoense S þþ
Armases angustipes S þ
Aratus pisonii S þ
Ocypodoids
Ucides cordatus L –
Uca (Leptuca) cumulanta S þþ
Uca (Minuca) thayeri S –
Uca (Minuca) rapax S –
Grapsoids/Ocypodoids 6/1
factors such as ecosystem resilience, its level of degradation and
connectivity with pristine areas, together with the aims of the
restoration program, must be addressed in order to choose be-
tween “passive“ or “active” restoration strategies (DellaSala et al.,
2003; Holl and Aide, 2011; Rey Benayas et al., 2008).
The high development reached by planted trees in our Restored
Area after 5 years shows that our intervention was successful for
mangrove recovering. R.mangle is a rapidly developing tree
(Ferreira et al., 2007; Ross et al., 2001), and our planted trees
showed higher average height than trees of the same age and
genera in restored mangroves around the world (Table 3). Scarcity
on biomass data, however, hinders comparisons. Comparison of
planted trees development with natural stands can be only
descriptive, due to differences in age between stands or unknown
age of natural ones. Plantations showed lower height, dbh and basal
area but higher density and tree richness than natural stands older
or of unknown age (Bernini et al., 2013; Proffit and Devlin, 2005).
However, differences in structure and biomass between planted
and natural stands are less significant in 50 years old mangroves
(Luo et al., 2010) or even earlier (Salmo III et al., 2013). Develop-
ment of trees in the Self-recovered Area was significantly lower
than in the Restored one, as shown by their lower tree diameter,
basal area and biomass. These parameters, mainly biomass, are
lower in the Self-recovered Area also in comparison to young
stands studied in the Caribbean by Fromard et al. (1998) with a
higher stem density of L. racemosa, and Ross et al. (2001) in a highly
R. mangle predominating stand (Table 3). Presence of dwarf trees
suggests that factors like low soil penetrability or accumulation of
sulfides at waterlogged soil (McKee, 1993) could have diminished
plant recruitment and growth in our Self-restored Area.
It is noteworthy that tree biomass would be greatly overestimated
if we used the allometric equation for mangroves developed by
Medeiros and Sampaio (2008) for the region, instead of developing
our own allometric equations. This underlines that biomass alloca-
tion is specific for each mangrove stand in question (Komiyama et al.,
2008) and emphasizes the need for further development of allo-
metric equations for mangrove stands of different developmental
stages during restoration. The equation produced in this work can be
used for future monitoring of the study areas.
The only parameter that was superior in the Self-recovered Area
was tree richness, where two species (R. mangle and L. racemosa)
were present, while only R. mangle was present in the Restored one.
This Rhizophoraceae was chosen to restore area by their high
growing and resistance to management, expecting the settlement
of other mangrove species later. However, evidences of high
Self-recovered Native
After Before After mangrove
þþ e þþ þþ
þþ e þþ þþ
þ þ þ þ
þþ e þþ þþ
þ e e þ
þþ e þþ þþ
þ – þ þþ
þþ þþ þþ þþ
þþ – þþ þþ
– þþ – –
6/3 1/2 5/3 6/3
propagules consumption by crabs appeared early after planting
(Ferreira et al., 2007), and R. mangle dominated this area due to a
heavy consumption of propagules mainly of L. racemosa and
A. schaueriana by G. cruentata and other Grapsoids (Ferreira et al.,
2013). Absence of such crabs in the Self-recovered Area allowed
the recruitment of L. racemosa. Since the beginning of the restora-
tion program, the Restored Area showed a full set of Grapsoid
species that have colonized from neighbor forest, and G. cruentata
density increased associated to rapid red mangrove canopy devel-
opment, shading and litter input. Oppositely to Restored, Self-
recovered Area started the experiment with low crab richness,
and the nearly full set of Grapsoids was only found 5 years after,
pondering that A. angustipes may have not been collected due to
cryptic nature of juveniles. Sun exposure, distance to native forest
and less penetrable sediment might have initially limited crab
occurrence in the larger Self-recovered Area, specially Grapsoids,
more tree dependent (Ashton et al., 2003; Bosire et al., 2004).
Hence, site pre-existent carcinofauna influenced the tree species
that established (Clarke and Kerrigan, 2002; Ferreira et al., 2013)
and this, in turn, influenced the fastness of increase of crab pop-
ulations, a pattern also observed by Bosire et al. (2003, 2004).
Restored Area showed a higher crab density of G. cruentata and
U. cordatus than Self-recovered one, despite crab density in both
experimental areas was lower than native forest, yet in 2013
monitoring. Bosire et al. (2004) also found that reforested stands
were similar to natural in crab diversity, with Rhizophora planted
forest showing higher density than natural at 5 years, which shows
the positive impact of reforestation in macrofaunal recruitment.
However, mud crabs populations at replanted sites delayed 16 years
in reach density of native forests in Philippines (Walton et al., 2007).
Ocypodoids U. cordatus and Uca (Minuca) thayeri are shade depen-
dent significant burrowers collected in our both areas when trees
developed canopy, so populations also appeared earlier in Restored
Area. Similar Brachyuran richness after 5 years of planting in both
areas shows that Brachyuran functional group may be considerably
resilient at mangrove degraded areas, albeit population densities
recovery might have a delay respect to richness return.
Ferreira (1998) and Ferreira and Sankarankutty (2002) showed
that R. mangle forests can contain the full set of mangrove soil Bra-
chyura irrespective of whether the single species is present or it is
mixed with the other mangroves (L. racemosa or A. schaueriana) at
the regional level. High crab richness under R. mangle canopy was
associated also to conditions for construct complex tunnels systems
between their roots (Abele, 1976; Ferreira, 1998; Ferreira and
Sankarankutty, 2002; Warner, 1969) showing an important
 A.C. Ferreira et al. / Ocean & Coastal Management 110 (2015) 38e45 43

Table 3
Data on mangrove trees in Human Restored, Self-recovered after disturbances and Natural mangrove stands. R., Rhizophora; L., Laguncularia; A., Avicennia. Dbh and height
values express means, except Medeiros and Sampaio (2008) which uses maximum heights. In Human Restored mangroves all data are propagule plantations, except Huber
(2004) which planted 2 year old seedlings. In Self-recovered and Natural mangroves all data are from neotropical region, including solely forests with predominance of
R. mangle and/or L. racemosa. Natural mangroves includes naturally developed stands that were not previously human cleared.

Country Reference Age of Forest type/tree species Height dbh Biomass Basal area
development (y) mean (m) (cm) (Mg ha) (m2 ha)

Human Brazil This work P 5 R. mangle 4.12 1.85 60.43 13.10

Restored Brazil Huber 2004 5 R. mangle 1.23 e e e
Brazil Menezes et al., 2005 5 R. mangle e e e e
Colombia Elster 2000 5 R. mangle e e e e
Cuba Padro
n 1996 5 R. mangle 1.78 1.85 e e
Mexico Herna
ndez et al., 2004 5 R. mangle e e e e
USA Goforth and Thomas 1979 5 R. mangle e e e e
Kenya Bosire et al., 2003 5 R. mucronata 2.90 e e 3.0
Thailand Aksornkoae 1996 5 R. apiculata 3.56 2.64 22.81 e
Vietnam Hong 1996 5 R. apiculata 4.09 3.03 e e
Thailand Macintosh et al., 2002 5 R. mucronata 3.82 3.37 e e
5 R. apiculata 3.73 2.73 e e

Self- recovered Brazil This work P 5 Young R. mangle L. racemosa. 3.22 1.75 18.19 9.99
USA Ross et al., 2001 5 R. mangle L. racemosa 4.04 e 56.02 13.54
A. schaueriana.

Natural Brazil Silva et al., 2007 P No data R. mangle L. racemosa 5.4 6.2 107.46 9.5
mangroves A. schaueriana
Brazil Medeiros and Sampaio 2008 No data R. mangle L. racemosa R.m e 14 e 105 14.1
A. schaueriana L.r - 18
Brazil Soares and No data R. mangle A. schaueriana 7.63 8.8 e 24.74
Schaeffer-Novelli 2005
L. racemosa A. schaueriana 7.7 7.5 e 11.30
R. mangle
Brazil Soares 1999 No data R. mangle L. racemosa 6.32 e e 14.81
A. schaueriana
Brazil Maia and Coutinho 2012 No data R. mangle A. schaueriana 8.77 z10.1 e 2.97
L. racemosa
French Guiana Fromard et al., 1998 5e6 Young stage L racemosa 7.7 e 71.8 20.6
French Guiana Fromard et al., 1998 3e4 Pioneer stage L. racemosa 3.5 e 31.5 13.70
Puerto Rico Golley et al. 1962a No data R. mangle 7,5 e 62.9 e
USA McKee and Faulkner 2000 >60 R.mangle L.racemosa 7.5 11.3 e 26.3
A. schaueriana
>50 R.mangle L.racemosa 7.4 11.4 e 28.2
A. schaueriana
a
USA Coronado Molina et al 2004 No data Dwarf/R. mangle 1.2 e 12.5 e
USA Ross et al., 2001 No data Dwarf/R.mangle 0.97 e 22.28 e
L.racemosa A. schaueriana

Biomass in “This work” was calculated using polynomial equations for Potengi mangroves, using dbh of mature trees in each area. Species that appear in bold are the pre-
dominant or unique in each site.
e no data.
P- data from Potengi River.
a
-data extracted from Komiyama et al. (2008).

structural role in the community. Studies also showed that stands
restored with Rhizophora spp. can support a crab density equivalent
or even higher than natural mangroves even in forests with higher
tree richness (Ashton et al., 2003; Bosire et al., 2004; Macintosh et al.,
2002; Walton et al., 2007). Data suggest that Rhizophora trees are by
themselves key species for mangrove carcinofauna diversity and
hence for forest community development, at least at Neotropics.
Evidences suggest that planting R. mangle resembles a common
succession pathway that results in the predominance of this species
in Neotropical mangroves. This species and L. racemosa are able to
grow in the same littoral areas (Delgado et al., 2001; Souza and
Sampaio, 2011). However, the most common pattern is the devel-
opment of nearly pure stands of R. mangle, due to predation, shade
intolerance and other factors operating on the other tree species
(Ferreira et al., 2013; Rabinowitz, 1978; Sousa and Mitchell, 1999).
Despite successional characterization of mangroves depends on
scale (Lugo, 1980; Alongi, 2009) R. mangle forest seems to be stable
and self-maintaining in the Neotropics (Ball, 1980; Duke et al.,
1998). It has been recognized that planting fast growing pioneer
tree species can be a strategy to accelerate forest recovery (Balke
et al., 2013). Data indicate that, at least for species poor neotrop-
ical mangrove assemblages, planting R. mangle seems to be a
shortcut for a rapid recovery in sites with high propagule con-
sumption or unstable or tide-sweeping substrates (Ferreira et al.,
2007, 2013). It might also be effective when restoration of
mangrove ecosystem functions is urgently needed (Bosire et al.,
2004; Ferreira et al., 2007).
For larger or Self-recovered areas, since with appropriate hy-
drologic and soil conditions, solutions such as promoting water-
borne propagules to reach littoral areas can be highly effective for
mangrove restoration (Kamali and Hashim, 2011; Lewis III, 2005). If
resources for active restoration are scarce, passive recovery can be a
successful low cost alternative for mangrove restoration that pre-
serves tree diversity and crab assemblages, although the return of
ecosystem features and invertebrate functional groups may be
slower. A mapping and protecting of areas able to self recover
would be a shortcut to restore degraded mangrove forests, mainly
in areas with low incidence of major stressor factors. Monitoring
needs to be maintained in such areas, to study and eventually
manipulate successional patterns.
44 A.C. Ferreira et al. / Ocean & Coastal Management 110 (2015) 38e45
5. Conclusions
Comparison between reforested and natural areas is a starting
point to reach forest restoration success, but it is impaired by
different stand ages. Calculations of biomass production can be
used to compare tree development in restored mangroves, but each
forest has their own features, and the use of specific allometric
equations need to be performed for long term assessment. Tree
development and biodiversity return together can give a more ac-
curate approach of forest management efficacy. Despite low tree
richness, restoration using R. mangle can be justified to accelerate
the recovery of functional groups, ecosystem services and high
biomass production. However, depending on conditions such as
high propagule predation and area size, mangrove self-recovery
can be a legitimate low cost alternative for mangrove restoration
with higher tree diversity. Crab assemblages need to be considered
in Neotropical restoration plans and their reestablishment can be a
good indicator of forest functionality. Crab assemblage reached
after several years a similar composition in assisted, naturally
recovered and undisturbed areas, showing the high resilience of
this important functional group.
Acknowledgments
Conselho de Aperfeiçoamento de Pessoal Superior (CAPES)/
PNPD provided a Post Doctoral grant to Alexander C. Ferreira and
CNPq provided a PQ grant to Gislene Ganade. We also thank Dr.
Fúlvio A. Morais Freire for his suggestions to improve statistical
analysis, and Leonardo D. R. da Silva, Handson D. Pimenta, Elisa V.
Gurgel, Alysson S. de Souza, Eduardo Silva, Iran M. Torres and
several planting volunteers for their valuable field assistance.
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