Effects of heavy rainfall on Thalassia testudinum beds

www.elsevier.com/locate/aquabot

Aquatic Botany 87 (2007) 189–195

Effects of heavy rainfall on Thalassia testudinum beds

Iliana Chollett a,*, David Bone b, Daisy Perez b

a Instituto de Tecnologıa y Ciencias Marinas (INTECMAR), Edificio Ciencias Basicas I, Segundo Piso, Universidad Simon Bolıvar,

Postal address 89000, Caracas 1080-A, Venezuelab Departamento de Biologıa de Organismos, Universidad Simon Bolıvar, 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 Koning

(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

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 Koning (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: [email protected] (I. Chollett).

0304-3770/$ – see front matter # 2007 Elsevier B.V. All rights reserved.

doi:10.1016/j.aquabot.2007.05.003

various kinds of disturbances on seagrass meadows, do not refer

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 Bjork (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

I. Chollett et al. / Aquatic Botany 87 (2007) 189–195190

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 108400–108580N and 688110–688200W (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

Fig. 1. Map of Morrocoy National Park and its surroundings, showing the four samp

Cuatro (TC). The inset at upper left shows the location of Venezuela and Morroco

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 (Perez, 2005). In this work, we

evaluated shallow (1–1.5 m) beds of T. testudinum at four

locations within the Park: Boca Seca (1084905500N;

6881401900W) and Tumba Cuatro (1085000400N; 6881503900W)

both mainly under oceanic influence and located in the East of

the Park, and Cano Capuchinos (1084905200N; 6881704900W) and

Las Luisas (1085102300N; 6881704000W) on the western side,

inside the semi-enclosed interconnected embayments (Fig. 1).

ling sites: Boca Seca (BS), Cano Capuchinos (CC), Las Luisas (LL) and Tumba

y N.P. relative to the Caribbean Sea.

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).

I. Chollett et al. / Aquatic Botany 87 (2007) 189–195 191

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 (1085303800N; 6882500600W, 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,

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

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. 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).

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.

Fig. 5. Multidimensional scaling (MDS) of the structural variables of Thalassia testu

1993–94 (*) to 2000 (*). Initial and final sampling date are shown, arrows indi

I. Chollett et al. / Aquatic Botany 87 (2007) 189–195192

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

biomass (between 575 and 1150 g m�2) compared to values

reported by CARICOMP (1997), which report values between

200 and 4000 g m�2 for the entire Caribbean (Zieman et al.,

1997).

dinum based on Euclidean distances at the four sites studied. Data from the years

cate temporal sequence.

I. Chollett et al. / Aquatic Botany 87 (2007) 189–195 193

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 Cano

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 Cano 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), Cano Capuchinos

(CC), Las Luisas (LL) and Tumba Cuatro (TC) at eight sampling dates.

Averages and standard deviations.

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 Cano 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 Cano 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 (Perez, 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 (Perez 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 (Perez, 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,

Fig. 7. Percentage of dead tissue (A), percentage of leaf biomass (B) and productivity (C) at Las Luisas CARICOMP station (1085103000N, 6881502500W) during

1993–2002. Averages and standard deviations (modified from Bone et al., 2001).

I. Chollett et al. / Aquatic Botany 87 (2007) 189–195194

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. Perez, 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 gestion para la

conservacion’’, financed by the Fondo Nacional para la

Ciencia y la Tecnologıa (FONACIT). We wish to express our

thanks to all the researchers who kindly allowed us to

examine their information and data, especially A. Martın and

J. Isea.

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