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2 Journal of Plant Ecology
affects spatially large area with its high magnitude and ampli- growth habit). Mangrove trees are greatly affected by large dis-
tude, e.g. cyclones, hurricanes, catastrophic flooding, etc.; turbances due to their large stature, but mangrove associates or
Dale et al. 1998) are now more intense and frequent than oc- non-mangrove species are relatively less affected by such
curred anytime in the past (Solomon et al. 2007). This altered disturbances because of their smaller stature (Bardsley 1985;
pattern of disturbances is likely to affect mangrove succession Baldwin et al. 1995; Smith et al. 1994). This inequality in
(Grindrod et al. 2002; Lugo 2008). Thus, it is not surprising that vegetation damage from a disturbance translates into higher
the species composition in post-disturbance mangroves differs propagule shortage for mangrove tree species than non-tree
from that prior to disturbance (sensu Lugo 2008). Importantly, mangrove associates and non-mangrove species. Presumably,
the species composition in post-disturbance mangroves mangrove-associate or non-mangrove species capitalizing on
appears to be characterized by high abundance of small stature the lower vegetation damage from disturbance and altered
mangrove, mangrove-associate and salt-tolerant non-man- ecosystem condition gain an upper hand in the recovered
grove species of herbs, shrubs and climbers (Baldwin et al. mangroves (Dahdouh-Guebas et al. 2005b). Inequality of
1995; Bardsley 1985; Brown 2007; Ferwarda et al. 2007; Lugo propagule availability among the two (tree and non-tree
2000; Paling et al. 2008; Roth 1992; Smith et al. 1994, 2009; species) will also influence the species composition of newly
Urquhart 2009). Although occurrence of mangrove-associate raised lands.
and non-mangrove species along the forest edges is a normal However, disturbance in an ecosystem often creates cascade
phenomenon in mangrove forests, an increasing abundance of of events (Peters et al. 2011), so that the effects of large distur-
these species in the forest interior is rather unusual (Brown bances on mangroves may not be limited to only propagule
cyclones) and recently experienced increased frequency of species to mangrove-associate or non-mangrove species. To
large disturbances (frequent large flooding and cyclones). test our conceptual model, we conducted a scenario testing
We argue that: (1) under normal disturbance regime, man- experiment with varying degrees of dispersal barrier
grove regeneration follows typical successional patterns, (1090%) and propagule limitation (1090%) and explored
e.g. pioneer mangrove species (and sea grasses) / mid serial their effects on dominance of mangrove species. We also
mangrove species / climax mangrove species. (2) Following explored the scenarios of mangrove formation when man-
high frequency of large flooding and cyclones, the effect of grove-associate species experience equal or less (one-half,
dispersal barrier due to biological invasion causing propagule one-third, one-fourth) dispersal barrier than large mangrove
limitation may facilitate shift in dominance of mangrove species.
4 Journal of Plant Ecology
A CONCEPTUAL MODEL OF MANGROVE (Fransworth 2000; Harun-or-Rashid et al. 2009), say St1.
Viable propagules germinate and seedlings of mangrove and
SUCCESSION mangrove-associate species occupy by cm and ca proportions
Vegetation development in normal conditions of the vacant habitat, respectively. Seedlings may experience
We will consider a mature mangrove stand comprising a man- density-dependent mortality (survivorship: Cm and Ca).
grove tree species, Sonneratia apetala Buch.-Ham (hereafter Although seedling banks are important in post-disturbance
referred to as mangrove species) and a mangroves-associate mangrove regeneration (Roth 1992), it is most likely that large
species, D. trifoliata (hereafter referred to as mangrove- disturbances affect seedling banks of both mangrove and
associate species), and limit the scope of this model to processes mangrove-associate species equally because of their small
relevant to increasing abundance of mangrove-associate stature. Therefore, we did not include this factor in the
species in mangroves (Fig. 2). conceptual model. Similarly, we assumed constant and equal
Let us consider that the mangrove stand has Mt mature density-dependant mortality for both species because we are
individuals of a mangrove species and At mature individuals primarily interested in dispersal barrier and propagule
of a mangrove-associate species at time t (see Table 1 for a list limitation.
of symbols). If fecundities of mangrove and mangrove- Taken together, the dominance of mangrove species over
associate species are Fm and Fa, the net propagule productions mangrove-associate species in the new (post-disturbance)
are MtFm and AtFa, respectively. These propagules will disperse habitat at time t + 1 can be expressed by their ratio (equation 1)
to newly raised lands or suitable vacant habitats in pre-existing or scaled dominance (equation 2, scale 01; >0.5 means
Figure 2: simplified schematics of a normal (A) versus an alternate pathway of mangrove succession (B). The grey and dark hatched areas in-
dicate occupancies of mangrove and mangrove-associate species, respectively. Arrows indicate propagule flow (solid arrow = uninterrupted flow,
broken arrow = interruption). The shaded areas at dispersal route indicate presence of invasive species. The bottom row indicates: mangroves are
more affected than mangrove associates in relation to disturbances (a), disturbance increases biological invasion (b), with increasing invasion,
propagule availability of mangrove species drops sharply but little effects on mangrove-associate species (c) and with increasing invasive-barrier,
occupancy of mangrove-associate species increases (d). The solid lines in the bottom panel indicate mangrove species and the dotted lines indicate
mangrove-associate species.
Biswas et al. | Post-disturbance succession in coastal mangroves 5
Mt Mature individuals at times t (number per area) For mangrove species 100
At For mangrove-associate species 20
Fm Fecundity (number of individuals per year) For mangrove species 500
Fa For mangrove-associate species 250
vm Propagule viability (proportion) For mangrove species 0.8
va For mangrove-associate species 0.8
Sm Propagules in the soil seed bank (proportion) For mangrove species 0
Sa For mangrove-associate species 0.1
Cm Per capita survivorship following density-dependent For mangrove species 0.9
Ca seedling mortality (proportion) For mangrove-associate species 0.9
am Propagule loss due to tidal washout and propagule For mangrove species 0.1
aa predation (proportion) For mangrove-associate species 0.1
bm Propagules blocked by invasive species (proportion) For mangrove species 0.10.9
ba For mangrove-associate species 0.10.9
Mt Fm vm f1 am + bm g1 ca Cm
Mt#+ 1 : A#t + 1 = : 2
Mt Fm vm f1 am + bm g1 ca Cm + At Fa va f1 aa + ba g + St 1 1 cm Ca
Under normal disturbance regime, mangrove species colo- Vegetation development and recovery following
nize first followed by mangrove associates (Das and Siddiqi large disturbances
1985), so that colonization of a mangrove-associate species Large disturbances (cyclones, hurricanes and high flooding)
may be constrained by habitat availability (1 cm), but colo- cause death and damage of mature mangrove (dm) and
nization of a mangrove species is unconstrained. In this con- mangrove-associate species (da). Only survived adults (1
dition, propagule losses for both species are approximately dm and 1 da) can produce seeds/propagules. Because high
equalbecause proportion of washed-out and predated prop- tidal surges associated with large disturbances washout
agules may be equal for both species (am = aa). There is no dis- more propagules than that after normal (low) tidal surges
persal barrier of invasive species that could affect propagule (Lugo 2000), soil seed bank can be important and species that
dispersal or seedling establishment of these two species differ- possess soil seed bank can have an advantage. Therefore,
ently (bm = ba 0). In addition, soil seed bank contribution is following large disturbances, the dominance of mangrove
very little, and we can exclude this factor. Under this condi- species over mangrove-associate species can be written as
tion, the dominance of mangrove species over mangrove follows.
associate will be as follows (equation 3).
Mt Fm vm Cm Mt Fm vm 1 dm f1 am + bm g1 ca Cm
Mt + 1 : At + 1 typical = : 3 Mt + 1 : A t + 1 = :
At Fa va 1 cm Ca At Fa va 1 da f1 aa + ba g + St 1 1 cm Ca
4
A mangrove species often produce large amounts of propa-
gule, and in a mangrove forest, the abundance of mangrove Previous studies have found that large disturbances
species are generally higher than that of mangrove-associate cause higher dm than da (Bardsley 1985; Baldwin et al.
species. In addition, the numerator in equation 3 is uncon- 1995; Smith et al. 1994), but they did not consider b (prop-
strained while denominator is constrained (1 cm). Taken to- agule blockage by invasive species). We suppose that the
gether, M:A is likely to be >1 and thus mangrove species proportion of propagules blocked by invasive species is
dominates over mangrove-associate species. higher for mangrove species (because of larger seeds) than
6 Journal of Plant Ecology
mangrove-associate species (bm > ba). If the previous state- species in recovered mangroves when mangrove species
ment holds, then, the portion of habitats colonized by the simultaneously experience higher (twofour times) propor-
mangrove species (cm) is likely to be relatively small and tion of affected vegetation (d) and higher dispersal barrier
mangrove-associate species may occupy a higher portion of (b) than mangrove-associate species.
vacant habitat for colonization (1 cm). Now the dominance
of mangrove species over mangrove-associate species will be
as follows.
RESULTS
Mt Fm vm 1 dm f1 am + bm g1 ca Cm When mangrove and mangrove-associate species were
Mt + 1 : At + 1 = :
fAt Fa va 1 aa + St 1 g1 cm Ca equally affected by large disturbances (dm = 2d), mangrove
5 species dominated (proportion of mangrove; >0.90), and this
pattern was consistent for most ranges of dispersal barrier by
invasive species (Fig. 3a). However, when mangrove
Note that in equation (5) (under large disturbance), the
species were more affected than mangrove-associate species
numerator is more constrained (dm, bm) than equation (3)
(dm > da), the proportion of mangrove species decreased
under normal disturbance regime. However, the denomina-
but remained high enough to maintain the dominance (pro-
tor is mostly unconstrained or getting a benefit (St 1).
portion > 0.5; Figs 3bd). Only in an extreme scenario of 90%
Thus, the values of M:A under this scenario is likely to be
affected mangrove vegetation against 22.5% affected
smaller than that in equation (3). If large disturbances are
Mt Fm vm 1 dm f1 am + bm g1 ca Cm
Mt + 1 : At + 1 feedback = :
fAt Fa va 1 aa + St 1 gCa
DISCUSSION
6
So far, the prediction of post-disturbance mangrove vegeta-
tion recovery has been made based primarily on the extent of
physical damage to vegetation and the associated change in
METHODS: A SCENARIO TESTING habitat conditions, suggesting that frequent large disturban-
ces markedly alter community structure and composition
EXPERIMENT (Lugo 2008; Smith et al. 1994, 2009). Our study supports this
We considered a hypothetical initial condition (Table 1) and general view. But our study for the first time demonstrates
estimated proportion of mangrove species in recovered that biological invasion is an important dimension in post-
mangroves in the following year of a large disturbance. We disturbance succession and must be considered in the predic-
considered two different scenarios of affected vegetation: tion of mangrove vegetation development and recovery after
(1) mangrove and mangrove-associate species are equally disturbance.
affected (dm = da) and (2) mangrove species are two, The susceptibility of mangroves to invasion is context
three and four times more affected than mangrove- dependent (Foxcroft et al. 2011), and therefore, the relative
associate species (dm = 2da, dm = 3da and dm = 4da). Within importance of biological invasion in mediating vegetation
each scenario of affected vegetation (d), we considered two succession will vary among mangroves. Connectivity of
different patterns of invasion barrier (b): (1) equal mangroves to terrestrial or freshwater habitats and the
blockage to propagules of both species (bm = ba) and (2) presence of invasive species in that habitats and anthropo-
disproportional blockage of propagules of mangrove and genic activities in and around mangroves are examples of
mangrove-associate species (bm = 2ba, bm = 3ba and bm = contexts that may confound susceptibility of mangroves to
4ba). Finally, we computed the proportion of mangrove invasion (Anastasiu et al. 2011; Biswas et al. 2007; Howard
Biswas et al. | Post-disturbance succession in coastal mangroves 7
and Harley 1998; Levin et al. 2001). For example, due to that well-designed empirical studies on disturbance-medi-
high aquatic-terrestrial connectivity and intense upstream ated patterns and processes of biological invasion and subse-
anthropogenic activities in the Sundarbans, susceptibility quent vegetation development are critical for further
of this forest to invasion is high and a large amount of verification of our findings.
invasive species may enter into this forest following large It is known that physical factors and dispersal barrier
disturbances (Fig. 1e; Biswas et al. 2007). Although there moderate mangrove species distribution at a continental scale
are numerous reports on the presence of floating invasive (Duke et al. 1998). Our study implicitly emphasizes the
species in mangroves (Howard and Harley 1998; Lugo importance of dispersal barrier and physical factors in
1998; Schmitz et al. 1993), the extent of invasion may not structuring mangrove species at local scale and suggests that
be as large as in the Sundarbans. The timing of a disturbance an invasive species by affecting propagule dispersal of
or an invasion event may be another determinant of post- mangrove and non-mangrove species can change post-
disturbance invasion: if a disturbance or an invasion event disturbance species composition and community dominance
occurs during monsoon (in the context of tropical climate), (Harun-or-Rashid et al. 2009; Schmitz et al. 1993). However,
excessive rainfall may lower the hurdle of salinity that an the relative importance of propagule dispersal may vary
invasive species otherwise encounters. For example, in the among types of succession (primary vs. secondary) (Friess
Sundarbans during the monsoon period, salinity drops close et al. 2011) and the places of colonization (river mouths vs.
to fresh water level (Wahid et al. 2007) and the exotic- riverbanks; forest edge vs. interior); thus, the role of biolog-
invasive species E. crassipes does not experience the usual ical invasion in mediating succession is complex and context
saline condition that restricts its invasion. We acknowledge dependent.
8 Journal of Plant Ecology
Our proposed conceptual model is an enormous simplifica- presence of an invasive species. These findings have impor-
tion of a complex reality in the land-sea interfaces and needs tant implications for practitioners in mangrove management
careful interpretation. For example, post-disturbance and restoration. Depending on the mangrove system and
hydrologic alteration (Lewis 2005) and spatial and temporal its susceptibility to invasion, management of invasive
dimensions of disturbances are important factors in deter- species in terms of removal of propagule dispersal barriers
mining mangrove succession, but we did not consider these and seedbed filters such as floating and ground-deposited
factors here. We believe that consideration of temporal debris may be required in concert with management of re-
dimension will amplify rather than reducing the interactive sidual vegetation (removal of affected vegetation) (Dale
effects of invasive species affecting mangrove succession if et al. 1998) and/or plantation of native mangrove species af-
large disturbances are frequent. It would be worthy to ter large disturbances. We cannot overemphasize the need
develop a full dynamic model to predict case specific patterns for empirical studies on the complexity of biological
in the future. invasion and its role on mangrove formation. We need this
In conclusion, our study highlights the complexity of understanding urgently in order to take informed manage-
post-disturbance vegetation development and recovery in ment decisions for the protection of our coastal greenbelts
coastal mangroves and puts forward an important missing that are so critical for the livelihood of coastal communities
dimension, biological invasion, into the context. Our results and their very existence in the face of large disturbances that
imply that similar levels of disturbances may have different are predicted to be increasingly common due to climate
consequences on mangrove vegetation recovery in the change.
Biswas et al. | Post-disturbance succession in coastal mangroves 9
in this paper are those of the authors, and not necessarily the opinions
of the UNEP-WCMC.
Conflict of interest statement. None declared.
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