Aquatic Botany 147 (2018) 34–42

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Aquatic Botany
journal homepage: www.elsevier.com/locate/aquabot

Growth and mortality of mangrove seedlings in the wettest neotropical T

mangrove forests during ENSO: Implications for vulnerability to climate
change
⁎
José M. Riascosa, , Jaime R. Canteraa, Juan F. Blanco-Librerosb
a
Grupo de Investigación en Ecología de Estuarios y Manglares, Sección de Biología Marina, Departamento de Biología, Facultad de Ciencias Naturales y Exactas,
Universidad del Valle, Calle 13 # 100-00, Cali, Colombia
b
Grupo de Ecología Lótica: Islas, Costas y Estuarios (ELICE), Instituto de Biología, Facultad de Ciencias Exactas y Naturales, Universidad de Antioquia, Calle 67 # 53-
108, Medellín, Colombia

A R T I C LE I N FO A B S T R A C T

Keywords: Assessing factors affecting growth and mortality of mangrove seedlings, the critical transition between propagule
Mortality dispersal and recruitment to the sapling state, is crucial to understand and predict the fate of mangrove forests in
Mangrove recruitment our changing climate. This work aimed to understand seedling’s responses to contrasting temperature and
El Niño-Southern Oscillation precipitation regimes and analyze consequences for the persistence of these ecosystems under expected climate
Estuaries
change scenarios. Growth rate and mortality of seedlings were monitored monthly in an array of mangrove
Biogeographic Chocó
forests located along a tidal and salinity gradient in the central Pacific coast of Colombia, one of the rainiest
places on Earth. Seedlings were monitored from January to December 2016, coinciding with a major El Niño
(EN) episode and the abrupt transition to La Niña (LN) conditions. Seedling growth rates were generally low and
observed spatial patterns generally mirrored interspecific differences in the tolerance to stress induced by
salinity and inundation levels. Seedlings in basin forests showed higher growth rates than those in riverine and
fringe forests. Mortality was not different among species and unexpectedly low, considering the rates reported in
the literature and the supposedly stressful conditions associated with the EN-LN cycle. According to our analyses
the magnitude of local anomalies in air temperature and precipitation throughout the EN-LN cycle can be
stronger than those expected locally for 2071–2100 in relation to global climate change. Current and expected
shifts in precipitation regimes seem the main macroclimatic drivers of ecological changes in mangrove forests
thriving in the Pacific coast of Colombia.

1. Introduction et al., 2008). Growth and mortality of seedlings leading to recruitment

Mangrove forests are comprised of a few specialized woody trees
thriving in tropical and subtropical brackish intertidal wetlands. The
seedling stage of mangrove trees represent the transition between
water-borne dispersal and recruitment to the sapling stage making it
the most critical life-stage (Krauss et al., 2008). Understanding the
biotic and abiotic factors influencing this transition, particularly under
different scenarios of climate change and variability is crucial. It is
currently known that mangrove recruitment is spatially structured,
because the mangrove forest is strongly influenced by environmental
gradients (López-Hoffman et al., 2007). Canopy gaps control light in-
cidence to the understory and therefore gap formation by climatic
disturbances and biological processes strongly influence establishment,
early development and persistence of seedlings (Clarke 2004; Krauss
is also controlled by a set of climatic factors operating at global, re-
gional and local scales (reviewed by Krauss et al., 2008). At local scales
growth and mortality of seedlings varies among ecological or physio-
graphic types of forest, because they differ in soil type, tide and salinity
regimes and hydroperiod, which determine how seedlings move, settle
and survive (Di Nitto et al., 2008; Krauss et al., 2008; Di Nitto et al.,
2013).
El Niño-Southern Oscillation (ENSO) is the most important signal in
the interannual variation of the ocean-atmosphere system, strongly
affecting coastal ecosystems along the Tropical Eastern Pacific (Seeliger
and Kjerfve, 2013). ENSO has changed its strength, frequency and
characteristics over past decades and it is projected to change under
different global warming scenarios (Wang et al., 1999; Timmermann
et al., 1999; Yeh et al., 2009). In tropical areas of South America,

⁎
Corresponding author.
E-mail addresses: jose.m.riascos@correounivalle.edu.co (J.M. Riascos), jaime.cantera@correounivalle.edu.co (J.R. Cantera), juan.blanco@udea.edu.co (J.F. Blanco-Libreros).

https://doi.org/10.1016/j.aquabot.2018.03.002
Received 28 September 2017; Received in revised form 22 January 2018; Accepted 16 March 2018
Available online 27 March 2018
0304-3770/ © 2018 Elsevier B.V. All rights reserved.
J.M. Riascos et al.
climate anomalies associated with ENSO affect regional rainfall, river
discharge and sediment transport to the ocean through teleconnections
(Vörösmarty et al., 1996; Restrepo and Kjerfve, 2000; Riascos, 2006,
Blanco, 2009). Such hydrological variability is probably the most im-
portant forcing function for tropical coastal marine ecosystems, parti-
cularly estuarine ecosystems, in Latin America, particularly along the
Pacific coast (Kjerfve et al., 2001; Riascos et al., 2008). Therefore, cli-
matic anomalies associated with El Niño and La Niña phases of ENSO
seem to be important, particularly for reproduction, dispersion and
recruitment in mangroves located in the Tropical Eastern Pacific (TEP;
Ecuador, Colombia, Panamá and Costa Rica).
Despite the past warnings on the disappearance of mangroves due to
growing anthropogenic pressures combined with climate change (Duke
et al., 2007), Alongi (2015) predicted that climate change will generally
have mild effects, with some negative effects for mangrove forest along
arid coasts, subsiding river deltas and small islands. He based his pre-
diction using the most recent global climatological forecasts of sea
surface temperature, oceanic pH, CO2 concentrations, sea level rise and
precipitation and salinity by the Intergovernmental Panel on Climate
Change toward the end of the century. However, little is known about
the effects of sub-decadal variability associated with ENSO, which can
be stronger than the expected long-term changes forecasted by the IPCC
for tropical regions, given the strong influence on freshwater runoff.
Recently, Banerjee et al. (2016) reported on the decline in the above-
ground biomass of a mangrove species in India related to decadal-scale
salinity alterations.
In 2015–2016 the TEP experienced one of the strongest El Niño on
record; it was popularly depicted as the “Super El Niño” (Zhai et al.,
2016; Ren et al., 2017). Globally, precipitation patterns changed, sea
surface temperature exceeded historical records for 12 consecutive
months and sea levels were driven ∼7 millimeters higher as warming
ocean water expanded.
Here we describe the dynamics of growth and mortality of man-
grove seedlings from Colombia’s Pacific pluvial and meso-tidal forests,
considered among the most luxuriant forests in the world (West, 1956),
during the latest El Niño warming episode. The aims of this study were
(i) to analyze spatial-temporal differences in growth and mortality of
mangrove species thriving in the study area, (ii) to estimate anomalies
in precipitation and temperature in Bahía Málaga, their relationship
with El Niño and La Niña episodes and compare the magnitude of these
anomalies with the expected variations under climate change scenarios
by 2071–2100; and (iii) to discuss the relevance of these findings for the
long-term persistence of Colombia’s Pacific mangrove forest.
2. Materials and methods
2.1. Study area
The study was performed in the Uramba-Bahía Málaga National
Park (hereafter Bahía Málaga), a south-facing bay located in the central
region of the Colombian Pacific coast (Fig. 1). The bay is a tectonic
estuarine system (Cantera et al., 2013) and it shows an array of coastal
formations including soft substrates, mud or sand bottoms, cliffs and
rocky shores. The Bay is located in a high rainfall area of the western
hemisphere receiving between 7000–11,000 mm of precipitation an-
nually (Restrepo et al., 2002). Because it is strongly influenced by the
Inter-Tropical Convergence Zone (ITCZ) (the low-pressure belt of the
ITCZ moves north and south between 10°N and 3°S) it passes over the
Bay resulting in two rain periods: April-June and September-November.
Water depth in the bay averages about 13 m, with a maximum depth of
40 m. Tides are semi diurnal, with a tidal range of 4.1 m, temperature
varies between 25 and 30 °C and salinity between 19 and 28 in the
mouth of the bay and 1.3 and 10 close to small rivers (Cantera et al.,
1998; Lazarus and Cantera 2007).
35
Aquatic Botany 147 (2018) 34–42
2.2. Sampling design
Five ecological types of mangrove forests (sensu Twilley et al., 1998)
distributed along a salinity gradient through the estuarine system were
selected for this study: Basin, Riverine I and II, Fringe I and II (see
Supplementary material 1 for details). These forests were monitored
monthly between December 2015 and December 2016. Three re-
plicated places were randomly chosen within each mangrove type, with
at least 200 m distance among them (Fig. 1). In each place two 78.5 m2
plots were established: a low-level water plot that was called “external”
and a high-level water plot called “internal”, so 30 plots were mon-
itored. Therefore, three sources of variability were considered in the
sampling design: forest type, position in the intertidal and time, thus
conforming a 5 × 2 × 12 sampling design. There was, however, an
important source of variability that could not be accounted for by the
sampling design: the mangrove species composition, which differed
among forest types, positions and plots. Therefore, spatial and temporal
variability was analyzed separately for each species (Mora oleifera,
Pterocarpus officinalis, Rhizophora spp., Pelliciera rhizophorae and Avi-
cennia germinans).
In each plot, between five and ten mangrove seedlings were ran-
domly selected, identified and tagged with a consecutive number using
adhesive plastic tape. Growth rate and mortality of mangrove seedlings
was monthly monitored. Mean growth rate (mm day−1) was estimated
by averaging differences in shoot length (from the top of the hypocotyl
to the top of the plant) from the previous month in each plot. Any
tagged seedlings which died were replaced by haphazardly selecting
and tagging individuals from those remaining in the plot. There are not
large gaps in the canopy of these forest that may influence growth and
mortality. However, structure, age and development do vary among
forest. Therefore, the Holdridge Complexity Index (HCI) was used as an
estimator of spatial structure and development of the mangrove forest.
The index was computed as:
sdbh
HCI =
1000
where (s) is the number of mangrove species, (d) the stand density, (b)
the basal area, and (h) mean height in each plot (see Blanco et al., 2001
for details and a discussion of this index). The ratio of sapling density
(RSD) i.e., the density of Trees 2.5–10 cm diameter at breast height with
respect to the total tree density was estimated as an indicator of forest
age or successional stage (Blanco et al., 2001). See supplementary
material 1 for estimations of these indices.
2.3. Taxonomic issues
Two species of Rhizophora (R. mangle and R. racemosa) occur in the
study area, with the former being much more abundant. They can be
identified in the adult stage using mainly the morphology of the in-
florescence, but these diagnostic characters are extremely plastic (see
Cerón-Souza et al., 2010). A reliable identification at the seedling stage
remains difficult, they are reported here as Rhizophora spp. Pterocarpus
officinalis (Fabaceae) was abundant in the study area. It is not con-
sidered a true mangrove species, but was included in our study because
it is tolerant to flooding and soil salinity, thus representing a transition
between forested wetlands and tidal mangroves in the Pacific and
Caribbean (Francis and Lowe, 2000; Medina et al., 2007). The con-
sideration of Mora oleifera (Leguminosae) as a true mangrove tree re-
mains controversial (e.g. Lacerda, 2002) but it was locally abundant and
was included in our monitoring.
2.4. Environmental data sources
Regional climate change scenarios for mean temperature and pre-
cipitation to 2071–2100 were provided by IDEAM (Instituto de
Hidrología, Meteorología y Estudios Ambientales, Colombia). These
J.M. Riascos et al. Aquatic Botany 147 (2018) 34–42

Fig. 1. Map of the study area in Bahía Málaga, Pacific coast of Colombia. The map shows the different mangrove forest types (see Appendix A) monitored and the
meteorological stations La Misión and Malaguita. Two plots (internal and external, see materials and methods) were monitored in each of the 15 sampling points. The
distribution of mangroves was plotted from the global distribution of mangrove forest derived from earth observation satellite imagery version 1.3 (Giri et al., 2011).

36
J.M. Riascos et al.
scenarios were built from the outputs of the Coupled Model
Intercomparison Project Phase 5 produced by the World Climate
Research Programme. IDEAM provided multi-model and multi-scenario
temperature and precipitation projections: 16 global climatic models
were selected and assembled, based on their relevance in a regional
context and projections were averaged for the distinct Representative
Concentration Pathways describing different 21st century pathways of
anthropogenic greenhouse emission scenarios (RCP2.6, RCP4.5,
RCP6.0, RCP8.5).
Moreover, data on the Oceanic Niño Index (three month running
mean of ERSST.v4 SST anomalies in the Niño 3.4 region) were gathered
from the Climate Prediction Center of the National Oceanic and
Atmospheric Administration, United States to describe anomalies re-
lated to the last El Niño-La Niña episodes. Finally, in situ data
(1969–2016) on monthly precipitation (mm) and monthly mean tem-
perature (°C) were gathered from IDEAM for two meteorological sta-
tions located close to the study area (Fig. 1). For temperature, data for
2016 were incomplete. Therefore, temperature data based on satellite
observations were obtained from the NASA Goddard Institute for Space
Studies (Global Modeling and Assimilation Office, 2015) and a com-
parison and correlation of in situ data versus satellite-based data was
used to estimate missing temperature data for 2016 (see Supplementary
material 2).
2.5. Data analyses
2.5.1. Between species comparisons
An analysis of covariance (ANCOVA) was used to assess the effect of
a categorical factor (mangrove species) on mean growth rate, control-
ling for the effects of two continuous covariates (HCI and RSD). Species
was treated as fixed factor. Mean growth rate was Log-transformed to
meet assumptions of the model concerning distribution or errors. Tukey
HSD test were conducted to assess specific between species differences.
A multiple logistic regression running under the Generalized Linear
Model approach implemented in “R” (R Development Core Team, 2008)
was used to determine if a categorical factor (species) and two con-
tinuous independent variables (HCI and RSD) are good predictors of
seedling mortality. The model used the binomial distribution for the
binary response variable (death: 1: alive: 0) and the Logit as the link
function. To test the model, we first fitted the full model involving all
the predictors and based on those results we fit a reduced model. Wald
tests were used to assess the significance of categorical factors. There-
after, we tested the significance of the final model using the likelihood
ratio test.
2.5.2. Species-specific spatial and temporal patterns in growth and mortality
To assess spatial and temporal differences in seedlinǵs growth rate,
an ANCOVA analysis was performed, using three categorical (fixed)
factors (type of forest, position in the intertidal and time). All the
higher-order interactive effects of factors were included in the model
when possible (i.e. some species did not occur in all type of forest/
positions/times). The HCI and RSD were included in the model as
covariates or continuous regressors. When a species occurred only in
one forest type, covariates were not included and standard ANOVA was
Table 1
Results of the ANCOVA analysis on the effects of categorical and continuous
predictors on the mean growth rate of mangrove seedlings. Significant factors
(α = 0.05) are printed in bold.
Effect SS DF MS F P
Intercept 0.757 1 0.757 49.318 < 0.0001
Species 3.267 4 0.817 53.221 < 0.0001
HCI 0.006 1 0.006 0.412 0.5211
RSD 0.017 1 0.017 1.090 0.2969
Error 6.829 445 0.015
37
Aquatic Botany 147 (2018) 34–42
conducted. Tukey HSD test were applied to assess differences between
species. As in the previous section, a multiple logistic regression was
used to determine if type of forest, position and time (categorical fac-
tors) and HCI and RSD (continuous predictors) are good predictors of
seedlings mortality. The model used the binomial distribution for the
response variable and Logit as the link function. The model was tested
using the likelihood ratio test, as mentioned before. Changes in tem-
poral patters were analyzed in light of local fluctuations of temperature
and precipitation during January-December 2016.
2.6. Local vs. regional ENSO anomalies
To calculate local anomalies in temperature and precipitation
during El Niño-La Niña, we followed a similar approach to that used by
the Climate Prediction Center (NOAA, United States) to calculate the
Ocean Niño Index1: we estimated the three-month running means of
temperature/precipitation “anomalies”, defined as the difference be-
tween the observed mean temperature/precipitation and the corre-
sponding monthly mean of a reference 10-year base period updated
every 5 years. Thereafter, we used a simple regression model (least
square fit) to test for the relationship (teleconnection) between tem-
perature anomalies described by the ONI and local anomalies observed
in the study area. The significance of the relationship (the regression
slope) was tested by an analysis of variance.
3. Results
3.1. Between-species comparisons of growth and mortality
The ANCOVA analysis showed that there were significant differ-
ences in growth rate of seedlings among mangrove species (Table 1).
Post hoc tests indicated that M. oleifera and P. officinalis grew sig-
nificantly faster than Rhizophora spp, P. rhizophorae and A. germinans
(Fig. 2). On the other hand, the spatial structure and development of the
forest and its demographic condition, as depicted by the HCI and RSD
respectively, were not significant as predictors of seedling growth rate
(Table 1).
Mortality of mangrove seedlings was low, Only 51 seedlings died
during the year. The mean mortality was 2.7% (4.1 seedlings per
month). The Wald test showed that, overall, species was not significant
(χ2(4) = 6.1; p = 0.19) as a predictor of the observed differences in
mortality. Among continuous predictors, only HCI was significant
(Table 2). Therefore, data were fitted to a reduced model that only
included this predictor. This suggest that in the array of mangrove
forest evaluated here the mortality of seedlings was higher in spatially
complex and developed forests.
3.2. Species-specific spatial and temporal patterns
3.2.1. Growth rate
There were significant differences in the growth rate of Rhizophora
spp. with space and time (Table 3). Growth rate was significantly faster
in Basin mangrove forest than in Riverine II and Fringe I forest
(Fig. 3A). On the other hand, growth rate was low in January, peaked in
February and decreased thereafter, with a small peak in July (Fig. 3B).
Neither the interaction term between type of forest and time nor the
covariates had a significant effect on the growth rate of Rhizophora sp.
Avicennia germinans seedlings were restricted to external plots in Fringe
II forest. There were significant temporal differences in growth rate
(Table 3): seedlings grew about one order of magnitude faster in March
in comparison with the rate observed between May and November
(Fig. 4A). P. rhizophorae occurred only in internal plots of Fringe I and
Fringe II mangrove forest. They grew significantly faster (almost twice)
1
http://www.cpc.noaa.gov/products/analysis_monitoring/ensostuff/ensoyears.shtml.
J.M. Riascos et al. Aquatic Botany 147 (2018) 34–42

Table 3
Results of the ANCOVA/ANOVA assessing the effects of categorical and con-
tinuous factors on the growth rate of seedlings of distinct mangrove species.
Significant factors (α = 0.05) are printed in bold.
Species/effect SS DF MS F P

Rhizophora spp.
Intercept 0.027 1 0.027 4.755 0.0302
Month 0.183 11 0.017 2.888 0.0014
Forest type 0.061 4 0.015 2.658 0.0336
Month × Forest type 0.266 44 0.006 1.051 0.3939
HCI 0.000 1 0.000 0.009 0.9247
RSD 0.020 1 0.020 3.481 0.0633
Error 1.346 234 0.006

Mora oleifera
Intercept 4.458 1 4.458 63.051 0.0000
Position 0.018 1 0.018 0.248 0.6290
Month 1.047 11 0.095 1.346 0.3237
Position × Month 0.496 11 0.045 0.638 0.7640
Error 0.707 10 0.071

Pelliciera rhizophorae
Intercept 0.365 1 0.365 62.299 < 0.0001
Forest type 0.028 1 0.028 4.803 0.0332
Fig. 2. Variability of mean growth rate of seedlings of different mangrove Month 0.038 11 0.003 0.590 0.8277
species (January to December 2016). Levels of the factors not connected with Forest type × Month 0.019 11 0.002 0.295 0.9837
the same lettering are significantly different after Tukey HSD tests (p < 0.05). Error 0.287 49 0.006

Avicennia germinans
Intercept 0.332 1 0.332 56.627 < 0.0001
Table 2 Month 0.299 11 0.027 4.630 0.0011
Coefficient estimates for the parameters of full and reduced logistic regression Error 0.129 22 0.006
models on the effects of species and continuous predictors on the mortality of
Pterocarpus officinalis
mangrove seedlings. AIC: Akaike information criterion. Significant factors
Intercept 3.988 1 3.988 184.766 0.0000
(α = 0.05) are printed in bold. Month 0.624 11 0.057 2.627 0.0117
Effect Estimate SE z Pr(> |z|) Error 0.928 43 0.022

Full model
Intercept −4.387 1.257 −3.489 0.0001
M. oleifera 1.390 1.166 1.192 0.2333
P. rhizophorae −0.461 1.180 −0.391 0.6957
Rhizophora spp. 0.421 1.043 0.404 0.6863
P. officinalis 0.382 1.173 0.326 0.7445
Holdridge Complexity Index 0.255 0.122 2.088 0.0367
Ratio of Staples Density 0.346 0.749 0.462 0.6441
AIC 459.160

Reduced model
Intercept −3.863 0.194 −19.931 < 0.0001
Holdridge Complexity Index 0.311 0.092 3.377 0.0007
AIC 455.320

in Fringe I than in Fringe II forest (Fig. 4B), but temporal differences

were not significant for this species (Table 3).
Seedlings of M. oleifera only occurred in basin mangrove forest, so
neither comparisons among forest types nor the correlation with HCI
and RSD were possible. The ANOVA analysis (Table 3) indicated that
although seedlings grew faster in internal plots were this species is
dominant, there were no differences in growth rate between internal
and external plots. Likewise, growth rate did not differ between months
(Table 3). P. officinalis seedlings were only found in external plots of
Basin forest, among seedlings of M. oleifera. Growth rate significantly
differed among months (Table 3), with faster growth observed in Feb-
ruary and slower growth in August and November (Fig. 4C).

3.2.2. Mortality
As there were no species-specific differences in mortality, the lo-
Fig. 3. Variability in the growth rate of Rhizophora spp. seedlings (A) among
gistic regression model was run again including forest type, position on forest types; (B) among months. Levels of the factors not connected with the
the intertidal and month along with HCI and RSD for all species. Results same lettering are significantly different after Tukey HSD tests (p < 0.05).
of this modeling showed that there were no significant spatial or tem-
poral effects on the observed mortality (Table 4). In contrast, HCI
showed again a significant effect on mortality, confirming our previous
analysis. This reduced model (only HCI as an explanatory variable)

38
J.M. Riascos et al. Aquatic Botany 147 (2018) 34–42

Fig. 4. Variability in the growth rate of mangrove seedlings. (A) Temporal variability in the growth rate of Avicennia germinans; (B) Differences in the growth rate of
Pelliciera rhizophora between forest types. C. Variability in the growth rate of Pterocarpus officinalis among months. Levels of the factors not connected with the same
lettering are significantly different after Tukey HSD tests (p < 0.05).

Table 4
Coefficient estimates for the parameters of full and reduced logistic regression
models on the effects of categorical and continuous predictors on the mortality
of mangrove seedlings. AIC: Akaike information criterion. Significant factors
(α = 0.05) are printed in bold.
Effect Estimate Std. Error z value Pr(> |z|)

Full model
Intercept −3.702 0.763 −4.850 < 0.0001
Riverine I −0.189 0.586 −0.323 0.7465
Riverine II 0.008 0.445 0.020 0.9843
Fringe I −0.490 0.513 −0.955 0.3396
Fringe II −1.309 0.768 −1.703 0.0885
Interior −0.165 0.322 −0.514 0.6071
January 0.231 0.575 0.402 0.6874
February −0.021 0.594 −0.036 0.9711
March −0.434 0.660 −0.658 0.5107
May −0.406 0.660 −0.614 0.5390
June −0.150 0.622 −0.242 0.8091
July −1.066 0.828 −1.287 0.1982
August −1.758 1.089 −1.614 0.1065
September −0.404 0.660 −0.613 0.5401
October −1.762 1.089 −1.617 0.1058
November −0.402 0.660 −0.610 0.5421
December 0.192 0.574 0.334 0.7380
HCI 0.317 0.131 2.420 0.0155
RSD 0.898 1.070 0.840 0.4009
AIC 469.050

Reduced model
Intercept −3.863 0.194 −19.931 < 0.0001
HCI 0.311 0.092 3.337 0.0007
AIC 455.300

performed significantly better than the null model (χ2(1) = 8.61;

p = 0.0033).
Species showing significant temporal differences in growth rates,
were plotted together with the Oceanic Niño Index and monthly mean
temperature and precipitation in the study area for comparisons
Fig. 5. Temporal changes in growth rates of seedlings in the context of local
(Fig. 5). A correlation analysis between growth rates vs. temperature
environmental variability during El Niño-La Niña 2016. (A) species showing
and precipitation showed that only P. officinalis had a significant, ne-
significant temporal variability in growth rates. (B) El Niño (black bars) – La
gative correlation with precipitation (r = −0.795, p = 0.002): growth Niña (white bars) episodes during 2016, as depicted by the Oceanic Niño Index.
rate was higher when the precipitation was low, coinciding with El (C) changes in mean air temperature and mean precipitation in Bahía Málaga.
Niño episode.

2.41–2.50 °C for the coastal zone. In contrast, annual precipitation will

3.3. Climate change, ENSO and local environmental anomalies
slightly decrease in the region, but no clear changes are expected in the
coastal area (-10% to 10%).
According to IDEAMs 2015 report on climate change for Co-
There was a significant relationship between ONI and local tem-
lombiańs regions, under the multi-scenario of global emissions of
perature (F1,254 = 462.994; p < 0.001) and precipitation
greenhouse gasses, the mean annual temperature in the central part of
(F1,253 = 57.647; p < 0.001) anomalies. The ONI accounts for ∼66%
the Pacific Coast of Colombia (Valle del Cauca region) will generally
of the observed temperature anomalies and ∼25% of precipitation
increase by the end of the 21th century, with an increase of

39
J.M. Riascos et al.
anomalies in the study area during El Niño and La Niña episodes
(Fig. 6A and B). During strong episodes (Fig. 6C), monthly mean tem-
perature in the study area can depart 1.55 °C above and 0.66 °C below
mean historical temperature during El Niño and La Niña, respectively.
In turn, precipitation can decrease up to 52% and increase up to 29% in
December in comparison with the historical mean during El Niño and
La Niña episodes, respectively (Fig. 6D). Therefore, the magnitude of
local anomalies observed during El Niño-La Niña cycle (∼2.2 °C in
temperature and ∼80% in precipitation) can be stronger than those
expected for 2071–2100 as affected by global climate change.
4. Discussion
In the context of expected effects of climate change on estuarine
systems the interest has focused on sea-level rise. It will likely have the
largest impact on coastal wetlands because inundation and salinity re-
gimes are key drivers of ecological and physiological processes in these
systems (Koch and Snedaker, 1997; Mitsch and Gosselink, 2007; Gilman
et al., 2008; Alongi, 2015; Armitage et al., 2015). Our findings on
spatial and temporal structure of growth and mortality of seedlings
largely mirror species-specific tolerances and responses to these para-
meters (Ball et al., 1997; Krauss et al., 2008) and the distribution of
different forest types along the salinity and tidal inundation gradient.
While fringe forests in Málaga Bay are exposed to frequent tidal in-
undation and salinities ranging between 19 and 28 ups, basin forests
close to small rivers are rarely inundated and salinity ranges between
1.3 and 10 (Cantera et al., 1998; Lazarus and Cantera, 2007)
The faster growth rate observed for seedlings of M. oleifera and P.
officinalis in comparison with those of Rhizophora spp, P. rhizophorae
and A. germinans seems to be related with the spatial distribution of
these species. M. oleifera and P. officinalis are restricted to basin man-
grove forests, thus being less exposed to tidal flooding with brackish
water and wave action. Life history traits in these forests seem to favor
seedlings having thin, fast-growing stems. A compilation of growth
rates of conspecific seedlings from reported literature (Supplementary
material 3) seems to support this view; growth rate of seedlings gen-
erally decreases from species occupying seaward edges (e.g. Rhizophora,
A. germinans) to species thriving in more elevated areas or landward
edges of mangrove forests (e.g. M. oleifera, P. officinalis). While light
levels and canopy structure strongly influence seedling growth (e.g.,
40
Aquatic Botany 147 (2018) 34–42
Fig. 6. Relationships between ENSO and local
climatic regimes. A and B) Linear regression
analysis of the relationship between the
Oceanic Niño Index during El Niño
(O.N.I. > 0.5) and La Niña (O.N.I. < 0.5) epi-
sodes and local anomalies in temperature
(La Misión station) and precipitation
(Malaguita station), respectively for the period
1969–2015; dotted line represents 95% con-
fidence interval. C and D) Monthly anomalies
in temperature and precipitation during strong
El Niño (st-EN) and La Niña (st/-LN) episodes,
as compared with historical data (1969–2015).
Episodes designed as “strong” were based on
the value of the Oceanic Niño Index; for El
Niño: May 1972 to March 1973, April 1982 to
June 1983 and March 1997 to May 1998; for La
Niña: June 1973 to July 1974, October 1984 to
June 1985 and July 1998 to March 2001.
Ball et al., 1997; Koch, 1997; López-Hoffman et al., 2007), differences
in structure and demographic stage of the forests included in this study
were not as strong as to influence seedling growth.
Mortality of seedlings, which did not differ among species, was low.
The accumulated number of dead seedlings (all species) reached ∼35%
during a year. This was unexpected, considering the particular en-
vironmental conditions during 2016 and the available field data on
annual rates of mortality of conspecifics elsewhere (Supplementary
material 3). In contrast with growth, mortality of seedlings was sig-
nificantly affected by the HCI; mortality was higher in more developed
and complex forests. This is in line with several studies showing an
influence of the canopy structure and light incidence on seedlings
mortality (e.g., Rabinowitz, 1978a; Sousa et al., 2003; López-Hoffman
et al., 2007). Moreover, the fact that HCI affected seedlings mortality
but not growth suggests that these processes are not necessarily cou-
pled, as observed by López-Hoffman et al. (2007) for A. germinans. The
lack of differences in mortality found in this study contrasts with
findings by Rabinowitz (1978b) in Panama, Ellison and Farnsworth
(1993) in Belize and Davis (1940) in Florida. They found that seedlings
of Rhizophora survive for more than a year, while those of Avicennia,
Laguncularia, and Pelliciera show lower survival rates and cohorts
usually die within 6 months.
Seedlings of R. mangle were by far the more abundant and occurred
in all forest types and intertidal positions. As such, spatial patterns were
clearer and growth rate was higher in forest with less exposure to tidal
flooding and salinity stress (Basin and Riverine I). This is in line with
previous findings on decreased stomatal conductance and chlorophyll
fluorescence, measures of photosynthetic activity, with increasing
salinity stress (Biber 2006). Seedlings of A. germinans in contrast were
restricted to external plots Fringe II forests, probably reflecting the
preference for relatively higher salinity observed in Avicenniaceae in
comparison with Rhizophoraceae (Downton, 1982; Hutchings and
Saenger, 1987; Lovelock and Feller, 2003). Occurring in internal
(landward) plots, seedlings of P. rhizophorae grew faster in Fringe I than
in Fringe II forests. As the main difference between these forests was the
RSD, describing the forest age or successional stage (see Appendix A), it
seems that growing conditions for seedlings of P. rhizophorae may be
more demanding in forests with a higher density of sapling.
The growth rate of M. oleifera did not show spatial or temporal
differences. This result should be taken with caution, because it could
J.M. Riascos et al.
be related with its restricted distribution (Basin forests) and low
abundance in our dataset. Although P. officinalis has been considered a
plant representing the transition between mangrove and terrestrial
forests (Francis and Lowe, 2000; Medina et al., 2007), it was abundant
only in external (seaward) plots in Basin forests, among seedlings of M.
oleifera and Rhizophora spp. and its growth rate displayed strong tem-
poral differences.
Giving the limited temporal scope of our data, it is difficult to
conclusively assess growth and mortality responses of seedlings to
changes in air temperature and precipitation. From the species showing
significant temporal differences in growth rate (Figs. 3 and 4), only P.
officinalis showed a significant correlation with these environmental
parameters. The beginning of our study coincided with the inflexion
point of strongest thermal anomalies associated to the El Niño episode
2015–2016, one of the strongest on records. By August 2016, conditions
had turned to La Niña episode, which lasted until the end of the year.
These shifting large-scale oceanographic conditions were reflected in
anomalously high temperature for most of the year and a deficit of
precipitation during the first half of the year, which turned in excess in
the second half. Hence, sublethal or lethal effects may be expected,
particularly considering high mortality rates reported in literature. As
this was not the case, we could infer that the seedling stage of man-
groves in this region can cope with local anomalous conditions asso-
ciated with ENSO extremes. Therefore, a larger dataset involving ENSO-
neutral periods is needed to objectively assess responses of growth rate
and mortality. It is noteworthy that no new seedlings recruited in the
plots being monitored in this study.
Our results show that, regarding temperature and precipitation, the
magnitude of local anomalies related to the ENSO cycle can be stronger
than those expected for the last part of the century in relation to global
climate change. As ENSO has been changing in strength and frequency
and this trend could continue under global warming (Timmermann
et al., 1999; Yeh et al., 2009; Wang et al., 2017) it brings up the
question: will mangrove ecosystems be resilient or resistant to these
mixed short-term and long-term climatic anomalies? Despite their
limited spatial and temporal extent, our results tend to support the
assertion that mangrove forests will either experience little change in
areas where precipitation is forecasted to increase (Alongi, 2015), at
least in hyper-humid mangrove forests. Regarding temperature and
precipitation, this prediction is based on the following facts or as-
sumptions: (i) for most mangrove species, rates of leaf photosynthesis
peak at about 30 °C and leaf CO2 assimilation decline at 30–35 °C (Ball
and Sobrado, 2002); temperature increases alone are likely to result in
faster growth, reproduction, photosynthesis, and respiration, changes in
community composition, diversity and an expansion of latitudinal
limits (Tittensor et al., 2010) and (iii) precipitation is largely seen as a
co-factor. Our historical dataset (1970–2016) on air temperature in the
study area, shows that the annual temperature averages 25.6 °C, with
little seasonal variation (25.1–26.1 °C) and that the highest monthly
mean on records was 28 °C (registered in March 1998, during El Niño
1997–1998). This suggests that temperature conditions are still in the
range that are supposedly favorable for mangrove growth, reproduc-
tion, photosynthesis and respiration. However, this seems a gross gen-
eralization made from scant evidence. According to Osland et al.
(2016), the vulnerability assessments of mangrove forest to climate
change is too focused on their ability to adjust to sea-level rise, but our
knowledge on temperature and precipitation regimes as macroclimatic
drivers of structure and function of mangroves is scant, and lags behind
that of terrestrial forests. Osland et al. (2017) identified 14 range limit
regions where temperature and precipitation regimes can cause abrupt
ecological transitions; they found that in the context of climate change,
changes in rainfall patterns are most likely to drive changes in structure
and function of mangrove forest in western South America. Therefore,
the results of this study provides baseline data to understand how
present and projected changes in temperature and precipitation regimes
are likely to affect the most critical life stage of mangrove forest
41
Aquatic Botany 147 (2018) 34–42
thriving in one of the rainiest places on Earth.
Author contributions
JMR, JFB, JRC conceived and designed the study. JMR carried out
the samplings, analyzed data and wrote drafts. JRC provided logistic
support. JFB, JRC reviewed drafts and provided insights. All authors
revised the final draft of the current manuscript.
Funding
Funding for this research was provided by Universidad del Valle.
This research was supported by a scholarship to JMR by the
Departamento Administrativo de Ciencia, Tecnología e Innovación
(Colciencias) − Programa “Tiempo de Volver”.
Conflict of interest
None.
Acknowledgements
We thank Juan Carlos Mejia for providing maps and plotted man-
grove coverage from satellite images processing. Thanks to the Consejo
comunitario de Comunidad Negra de La Plata Bahia Málaga for their
hospitality and for allowing access to their territory. Thanks to
Willington Aguirre, Diego Morales, Charlotte Hopfe for their help in
field work.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the
online version, at https://doi.org/10.1016/j.aquabot.2018.03.002.
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