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Effects of heavy rainfall on Thalassia testudinum beds

Article  in  Aquatic Botany · October 2007

DOI: 10.1016/j.aquabot.2007.05.003

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 Aquatic Botany 87 (2007) 189–195
www.elsevier.com/locate/aquabot

Effects of heavy rainfall on Thalassia testudinum beds

Iliana Chollett a,*, David Bone b, Daisy Pérez b
a
Instituto de Tecnologı́a y Ciencias Marinas (INTECMAR), Edificio Ciencias Básicas I, Segundo Piso, Universidad Simón Bolı́var,
Postal address 89000, Caracas 1080-A, Venezuela
b
Departamento de Biologı́a de Organismos, Universidad Simón Bolı́var, Postal address 89000, Caracas 1080-A, Venezuela
Received 13 March 2006; received in revised form 2 May 2007; accepted 15 May 2007
Available online 2 June 2007

Abstract
In December 1999 heavy continuous rains that lasted one week affected the Venezuelan coastline. At Morrocoy National Park, a large marine
reserve, rainfall values surpassed previous 32-year records and led to a decrease of salinity to 3 psu, which lasted for over a month at some
locations. This study examined effects of these changes on the shallow-water meadows of the seagrass Thalassia testudinum Banks ex Köning
(1805), by comparing their structure before and after this disturbance at four selected sites. The rain acted as a pulse-type disturbance, altering the
physicochemical features at all sites, which soon returned to the previously prevailing conditions. However, T. testudinum beds showed a sudden
stress reaction followed by slow recovery. The disturbance prompted an increase in the amount of dead tissue and defoliation. Later a sustained
increase of leaf biomass, productivity and reproductive shoots was observed, neither ever noticed before in the Park. The seagrass meadows in
Morrocoy showed signs of stress even one year after the impact, suggesting that the 1999 disturbance deeply affected the characteristics of these
systems within the Park.
# 2007 Elsevier B.V. All rights reserved.

Keywords: Caribbean; Venezuela; Disturbance; Rain; Seagrass bed; Thalassia testudinum

1. Introduction various kinds of disturbances on seagrass meadows, do not refer

Many natural or anthropogenic changes may induce
disturbances on marine ecosystems. Among them, rainfall is
usually an acute, pulse-type disturbance (Connell, 1997) that
may be regarded as an important disturbing factor, affecting
extensive coastal areas and altering their physicochemical
characteristics (i.e. salinity, temperature and turbidity). The
seagrass Thalassia testudinum Banks ex Köning (1805) exhibits
narrow ranges of physiological tolerance to changes in salinity,
with an optimum salinity range between 24 and 35 psu
(Zieman, 1975). A decrease in salinity is a stress factor that
induces physiological responses and alters quantifiable features
of population structure, biomass, morphometry and productiv-
ity (Zieman, 1975; Irlandi et al., 2002; Kahn and Durako,
2006).
Although transient increases of rainfall are common, few
studies have examined their effects on marine seagrasses. Short
and Willie-Echeverria (1996), in their review on the effects of
* Corresponding author. Tel.: +58 2 9063416; fax: +58 2 9063416.
E-mail address: iliana@intecmar.usb.ve (I. Chollett).
0304-3770/$ – see front matter # 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquabot.2007.05.003
to any study regarding the influence of rainfall or salinity.
Research on the effects of salinity on marine plants has been
restricted to estuarine populations (McKee and Mendelssohn,
1989; Flynn et al., 1995; Baldwin and Mendelssohn, 1998;
Zieman et al., 1999). However, some studies have evaluated
hyposalinity effects on marine plants. Zieman (1975) studied
the response of seagrasses exposed to effluents, causing drastic
changes of temperature and salinity, and Irlandi et al. (2002)
evaluated seagrass meadows affected by freshwater flows that
have altered the local turbidity. The effects of rainfall have been
examined together with other disturbance agents such as
mechanical stress (Orth and Moore, 1983) or the influence of
pathogens, turbidity, hypoxia and sulphur toxicity (Zieman
et al., 1999). Besides, in a few cases, hyposalinity effects on
seagrasses have been studied under laboratory conditions. For
example, Hellblom and Björk (1999) found that seagrasses
respond negatively to salinity decreases below an optimum
level and that this environmental parameter strongly influenced
the photosynthetic response of these submersed plants. Kahn
and Durako (2006) observed that hyposalinity conditions where
detrimental for the fitness of T. testudinum seedlings. Such
findings emphasize the importance of salinity fluctuations on
190 I. Chollett et al. / Aquatic Botany 87 (2007) 189–195

the performance of marine plants in the field, regardless of other
factors that may enhance or modify such effects.
This study reports on the effects of an unprecedented rainfall
event and the subsequent recovery of T. testudinum beds in a
coastal marine sanctuary area in Venezuela. Our aims were to
characterize the meteorological disturbance and assess its effect
on water quality and seagrass performance. These results were
compared with data previously collected at the same sites (Isea,
1994), which we used as an historical baseline.
2. Materials and methods
2.1. Locations
Morrocoy National Park is a coastal protected area located
on the northwestern coast of Venezuela, between 108400 –
108580 N and 688110 –688200 W (Fig. 1). The Park stretches over
320 km2 and comprises a system of loosely interconnected
lagoons opening to the sea through several channels. The Park’s
climate is chiefly savanna showing little seasonal changes; air
temperature varies between 25 and 30 8C, sea surface
temperature ranges from 26 to 29 8C and salinity usually
remains between 30 and 38 psu (Bone et al., 1998) although
major drops of the latter have been recorded after rainy periods
(Laboy-Nieves et al., 2001). Freshwater inflow into the system
relies on the discharges of seasonal creeks from the westerly
side of the Park and on the seasonal rainfall, which shows an
annual average of 1127 mm and two peaks, one from April to
May and a maximum towards the end of the year (Bone et al.,
1998).
Seagrass beds of T. testudinum are predominant in the inner
shallower embayments. The meadows are very heterogeneous
and change their structural characteristics in function to the
proximity to the open sea and the differential influence of
physicochemical factors (Pérez, 2005). In this work, we
evaluated shallow (1–1.5 m) beds of T. testudinum at four
locations within the Park: Boca Seca (108490 5500 N;
688140 1900 W) and Tumba Cuatro (108500 0400 N; 688150 3900 W)
both mainly under oceanic influence and located in the East of
the Park, and Caño Capuchinos (108490 5200 N; 688170 4900 W) and
Las Luisas (108510 2300 N; 688170 4000 W) on the western side,
inside the semi-enclosed interconnected embayments (Fig. 1).

Fig. 1. Map of Morrocoy National Park and its surroundings, showing the four sampling sites: Boca Seca (BS), Caño Capuchinos (CC), Las Luisas (LL) and Tumba
Cuatro (TC). The inset at upper left shows the location of Venezuela and Morrocoy N.P. relative to the Caribbean Sea.
 I. Chollett et al. / Aquatic Botany 87 (2007) 189–195
2.2. Sampling and analyses
A time-series analysis of the historical records of rainfall in
the Park was performed on the data from Santa Rosa
Meteorological Station (108530 3800 N; 688250 0600 W, data pro-
vided by the Ministerio del Ambiente y los Recursos Naturales,
MARN), which is located about 10 km NW of Morrocoy N.P.
At the 4 sampling stations and at another 16 along the Park the
sea surface temperature, salinity, pH and dissolved oxygen
were determined using a multipurpose Hydrolab DS4 Probe;
total suspended solids were measured according to the APHA
(1985) methodology, Sections 209-C and D. All these
measurements were carried out once a month over a 1-year
period after the rain episode.
The T. testudinum beds were sampled quarterly in February,
May, July and October 2000. The methods followed were those
recommended by the CARICOMP (2001) protocol for total and
fractional biomass, shoot density and productivity. Each sample
consisted of four replicates taken for biomass, using a PVC
corer of 15 cm internal diameter (=0.07 m2) and 40 cm depth,
and four additional replicates for productivity using 10 by
20 cm (=0.02 m2) quadrats. The growth of T. testudinum was
measured as the production of new leaf biomass. Leaf growth
was measured by marking all the leaves of the shoots inside the
quadrat at the green-white interface using a stapler. The
samples were collected 8–12 days later, harvesting the entire
shoot from the sediment.
Once collected, the samples were cooled and transported to
the laboratory for their separation in fractions. Biomass
samples were divided into four separate fractions: green
leaves, non-green leaves with short shoots, rhizomes and roots
and dead tissue. The leaves of the productivity samples were
clipped at the green-white interface and separated into three
fractions: new leaves, without marks, old growth; marked
leaves underneath the mark and old standing crop, marked
leaves above the mark. In each sample, the shoots with flowers
or fruits were counted, and the percentage of reproductive
shoots was calculated.
After separating the plants all the remaining sediment was
removed and the epiphytes were detached by briefly submer-
ging the leaves in 10% hydrochloric acid for not more than
5 min. Then, all the material was dried at 60 8C to constant
weight and quantified. Leaf productivity (the amount of new
material produced per unit area per day) was obtained by
summing up the total plant growth (new leaves plus old growth)
and dividing by the number of days (CARICOMP, 2001).
The same sampling sites had been studied 7 years earlier
using similar methods and timetables (June, September and
December 1993 and March 1994; Isea, 1994), thus rendering
comparable information between the two studies and allowing
us to use these earlier data as a historical reference baseline.
2.3. Statistical analyses
Differences in the intensity of the rainfall were evaluated
using t-tests. Principal Component (PC) analyses were applied
to the physicochemical data corresponding to January 2000,
191
July 2000 and January 2001 in order to detect any change
between dates, the relationships between the various sampling
stations and the presence of similar groups of stations. These
three dates reflect the general temporal trend of the data, and
allows a clearer and simplified picture of the physicochemical
temporal variations.
A Pearson correlation analysis was applied to the plant
variables: productivity, shoot density, total biomass and the
biomass of the different fractions in order to determine the
least-redundant variables ( p < 0.05) and incorporate them in
ulterior analyses. In order to compare the T. testudinum beds
between the year 2000 and the preceding period (1993–94),
results were arranged according to a multidimensional scaling
(MDS) model based on the Euclidean distance index for the
non-redundant and previously standardized parameters
obtained from the correlation analyses. Goodness-of-fit was
expressed by a stress value, which allows evaluation of how
well the resulting arrangement reflects the original similarities
in the specified dimensionality. The ANOSIM analyses were
then applied to evaluate differences between years or sampling
sites by means of calculations of the R-statistic and its
associated probability value (Clarke, 1993). Finally, the non-
parametric Kruskal–Wallis test was used to determine the
significance of changes of the most important variables prior
and after the rain event.
3. Results
3.1. Characterization of the event
December 1999 rains were significantly higher than any
previously recorded value within the Park (Fig. 2; t-test,
p < 0.05). The value was 34% higher than the next highest
value (in December 1970) surpassing the historical means for
that month by up to 5.5 times.
The Principal Component analyses of the physicochemical
variables of the waters from Morrocoy N.P. revealed that the
first two PC’s accumulate 66% of the total variance. The first
PC axis was related primarily by salinity (negative relationship)
and dissolved oxygen, and the second axis comprised
information related to temperature (Table 1). The PCA plot
(Fig. 3) displays substantial differences between sampling
Fig. 2. Monthly rainfall in mm, from 1968 to 2000. Mean  S.D. of monthly
values: 93.4  105.0 mm; broken circles indicate peaks above 600 mm. Data
from the meteorological Station Santa Rosa (Ministerio del Ambiente y los
Recursos Naturales, Venezuela).
192 I. Chollett et al. / Aquatic Botany 87 (2007) 189–195

Table 1
Principal Component (PC) analyses of the physicochemical variables at Mor-
rocoy National Park: component eigenvalues and the factor coordinates of the
variables determined for the first three PC
PC 1 PC 2 PC 3
Eigenvalue 2.14 1.17 0.84
Proportion 0.43 0.23 0.17
Cumulative 0.43 0.66 0.83
Variable
Temperature 0.01 0.82 0.31
Salinity 0.58 0.09 0.38
Dissolved oxygen 0.57 0.16 0.40
Total suspended solids 0.37 0.53 0.46
pH 0.45 0.14 0.63 Fig. 4. Multidimensional scaling (MDS) of the structural variables of Thalassia
testudinum based on Euclidean distances for the samples taken on eight
different dates. Separations according the year of sampling, showing 95%
confidence ellipses. Stress = 0.08.

months. Also, overall scatter declines from January 2000 to

January 2001. These differences are probably related to low
salinity values immediately after the rains (25.1  5.8 psu) and
their return to normal values (40.7  1.0 psu). The plot also
show the cyclic temperature pattern reported for the area (Bone
and Klein, 2000), with upper limits in summer (July 2000) and
lower limits in winter (January 2001).

3.2. Alterations of the Thalassia testudinum beds

The T. testudinum beds studied were of intermediate

Fig. 3. Marine sampling stations (20 sites) at Morrocoy N.P. Their physico-
chemical features are drawn on the surface defined by the first and second
Principal Components, and correspond to data from monthly means (*),
January 2000 (*), July 2000 (^) and January 2001 (4).
biomass (between 575 and 1150 g m2) compared to values
reported by CARICOMP (1997), which report values between
200 and 4000 g m2 for the entire Caribbean (Zieman et al.,
1997).

Fig. 5. Multidimensional scaling (MDS) of the structural variables of Thalassia testudinum based on Euclidean distances at the four sites studied. Data from the years
1993–94 (*) to 2000 (*). Initial and final sampling date are shown, arrows indicate temporal sequence.
 I. Chollett et al. / Aquatic Botany 87 (2007) 189–195
The correlation tests indicated that total biomass, produc-
tivity and percentage dead tissue were the non-redundant
variables useful for multivariate analyses. Based on these an
evident difference emerged when comparing the samples from
the two periods studied (Figs. 4 and 5); this difference was
highly significant (ANOSIM analysis, R = 0.732, p < 0.001).
A clear distinction exists between the first and the second
sampling period, as the populations apparently underwent
important changes. The differences between the two
periods were significant for all stations (ANOSIM analysis,
p < 0.05).
We found the highest quantities of dead tissue at Caño
Capuchinos, Las Luisas and Tumba Cuatro in February 2000
(Fig. 6). This difference was significant at Las Luisas (Kruskal–
Wallis test, p < 0.05). In 1993 the average leaf biomass
represented 16–24% of total biomass at all sampling sites; in
the year 2000 this fraction decreased to 9–16%, with significant
differences at Las Luisas and Tumba Cuatro between the two
periods (Kruskal–Wallis test, p < 0.05). Exceptionally low
values were recorded at Caño Capuchinos in February 2000 but
a fast recovery at this site rendered the annual comparison non-
significant. Mean productivity was higher at all stations in the
Fig. 6. Total biomass (dead tissue, DT and leaf biomass, LB) (A) and
productivity (B) at the four sites studied: Boca Seca (BS), Caño Capuchinos
(CC), Las Luisas (LL) and Tumba Cuatro (TC) at eight sampling dates.
Averages and standard deviations.
193
year 2000. The differences between the two periods were
significant at Boca Seca, Las Luisas and Tumba Cuatro
(Kruskal–Wallis test, p < 0.05), the increase ranging from 63 to
179%, with rapid rises at Caño Capuchinos and Tumba Cuatro
at the beginning of 2000. For the rest of this latter year the
values remained above the means registered in 1993–94, except
at Caño Capuchinos, which dropped to normal levels in
November 2000.
During the sampling, one noteworthy observation was made:
the appearance of 2% of reproductive shoots in July 2000, while
such were absent from the previous and later samples.
4. Discussion
In stressed aquatic plants the disturbance response is
characterized by an alarm phase that is followed by a restitution
one (Larcher, 1995). Zieman et al. (1999) observed that under
saline stress, Thalassia spp. leaves die and seagrass beds reduce
their total biomass through defoliation, until density-dependent
regulatory mechanisms increase the leaf tissue to an
approximate steady state (Van Tussenbroek et al., 2000). In
the same way, at Morrocoy N.P. T. testudinum populations
reacted to the perturbation through defoliation and die back.
Subsequently, seagrass beds recovered with a stimulation of
foliar production surpassing previous values, a typical response
of surviving shoots within disturbed patches (Gallegos et al.,
1992; Durako, 1994). As a result, leaf biomass increased during
the year of this study and the following one (Pérez, 2005).
However, in spite of these signs of recovery, the seagrass beds
in Morrocoy N.P. maintained a rather high productivity even a
year after the rains, suggesting that the seagrasses had not
completely recovered yet.
The differences observed in the seagrass beds in Morrocoy
N.P. could be attributed just to a long-term tendency in the data,
or an artifact of the dates sampled. This is a problem when there
are compared two groups of dates in time. However, in
Morrocoy, the CARICOMP program carries out a permanent
seagrass sampling scheme (Bone et al., 2001), which has a
continuous record of structural parameters of T. testudinum at
the CARICOMP station at Las Luisas bay. This record shows a
long-term stability in the structural parameters of the seagrass
beds in Morrocoy (Fig. 7), showing only two anomalous
periods inside the time series (1997 and 2000). These periods
were characterized by low values of leaf biomass and high
values of dead tissue and productivity. The first, early 1997,
agree with a meteorological disturbance over Morrocoy N.P. in
December 1996. In that month, the Park was affected by heavy
rainfalls (540 mm) that caused visible damage to the seagrass
beds, which recovered in just 5 months (Pérez and Galindo,
2000). Nonetheless, the magnitude of the damage on the T.
testudinum beds in Morrocoy N.P. during 2000 seemed to be
greater – even leading to the temporary disappearance of some
of the seagrass beds within the Park (Pérez, 2005) – and last
longer than previous findings. Although generally the recovery
of these plants begins as soon as the physicochemical
conditions return to their optimum (Zieman, 1975), in
Morrocoy the return to the initial state was very slow,
194 I. Chollett et al. / Aquatic Botany 87 (2007) 189–195
Fig. 7. Percentage of dead tissue (A), percentage of leaf biomass (B) and productivity (C) at Las Luisas CARICOMP station (108510 3000 N, 688150 2500 W) during
1993–2002. Averages and standard deviations (modified from Bone et al., 2001).
suggesting that the seagrass beds were exposed to a very intense
perturbation.
The maintenance and expansion of seagrass meadows
proceeds through vegetative growth and sexual reproduction.
Some authors state that flowering is a secondary mechanism in
the growing of these clonal plants (i.e. Gallegos et al., 1992),
however, several studies have found frequent sexual reproduc-
tion in many seagrass species (i.e. Olesen et al., 2004).
Apparently, the relative contribution of these two growing
modes depends of the species (Campey et al., 2002) or the
environmental conditions (Durako and Moffler, 1987; Gallegos
et al., 1992). In Morrocoy N.P. the role of sexual reproduction to
meadow maintenance seems to be very small, and T. testudinum
flowering has been an episodic event, recorded only two times
in 10 years of continuous observations (D. Pérez, personal
communication): in 1997 and 2000, after the two major
perturbation events occurred in the area. So, in Morrocoy,
flowering seems to be a stress response, in agreement with
earlier observations of Durako and Moffler (1987), Gallegos
et al. (1992) and Plus et al. (2003), highlighting the profound
impact of these heavy rains over the seagrass beds within the
Park.
Acknowledgements
This study was part of a larger research entitled ‘‘Estudio
Integral del Sistema del Parque Nacional Morrocoy con
miras al desarrollo de planes de uso y gestión para la
conservación’’, financed by the Fondo Nacional para la
Ciencia y la Tecnologı́a (FONACIT). We wish to express our
thanks to all the researchers who kindly allowed us to
examine their information and data, especially A. Martı́n and
J. Isea.
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