Increase in Straight and Coiled Cylindrospermopsis raciborskii (Cyanobacteria) Populations under Conditions of Thermal De-Stratification in a Shallow Tropical Reservoir

doi:10.4236/jwarp.2011.34031

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Journal of Water Resource and Protection, 2011, 3, 245-252

doi:10.4236/jwarp.2011.34031 Published Online April 2011 (http://www.scirp.org/journal/jwarp)

Increase in Straight and Coiled Cylindrospermopsis

raciborskii (Cyanobacteria) Populations under

Conditions of Thermal De-Stratification in a Shallow

Tropical Reservoir

Maria do Carmo Bittencourt-Oliveira1,2*, Ariadne do Nascimento Moura3,

Talita Caroline Hereman1,2, Enio Wocyli Dantas3,4

1Universidade de Sã o Paulo, ESALQ, De p. C i ênci as Bi ol ó gic as , Av. Pádua Dias, Piracicaba, Brazil

2Programa de Pós-Gra duação em Ciências Biol ó gic as, Área de Bi ol o gia Veget al,

UNESP-Rio Claro, Rio Claro, Brazil

3Universida de Fed eral Rural de Pern a m buco, Departamento de Biologia-Área de Botânica,

R. Dom Manuel de Medeiros, s/n, Dois Irmãos, Recife, Brazil

4Universidade Estadual da Paraíba - UEPB - Campus V, Centro de Ciências Biológicas e Sociais

Aplicadas-CCBSA, R. Monsenhor Walfredo Leal, nº 487, Tambiá, João Pessoa, Brazil

E-mail: [email protected]

Abstract

In recent decades, there have been frequent occurrences of the cyanobacterium Cylindrospermopsis

raciborskii in northeastern Brazil. Little is known regarding the response of straight and coiled morphotypes

to environmental conditions such as light intensity and water temperature. Samples were collected at the

Mundaú reservoir (PE, Brazil) at six sampling depths in the dry and rainy season. Both morphotypes

exhibited seasonal and vertical differences in densities. The reservoir was stratified in the dry season, with a

predominance of the straight morphotype. The coiled morphotype exhibited greater densities in the lower

strata and prove to be more susceptible to light. There was evident thermal de-stratification in the rainy

season, with a predominance of the coiled morphotype in the surface layers. Thermal de-stratification favors

an increase in both morphotypes by providing adequate conditions for growth, such as low light intensity and

milder temperatures, which are characteristic of the winter season in the northeastern Brazil.

Keywords: Cyanophyta, Light, Morphotype, Northeastern Brazil, Mundaú Reservoir

1. Introduction

In recent decades, the occurrence of cyanobacterial

blooms, such as those of the genera Microcystis Kützing

ex Lemmermann, Anabaena Bory ex Bornet & Flahault

and Planktothrix Anagnostidis & Komárek, have become

a common event in different regions of the world and are

closely related to eutrophication processes in aquatic

ecosystems. The presence of cyanobacterium in freshwa-

ter ecossystems are often associated with eutrophic con-

ditions, CO2 availability and high temperatures [1] low

luminosity [2], alkaline pH [3], high concentrations of

nutrients, especially phosphorus [4] and a low N:P ra- tio

[5], and buoyancy regulation [6]. Such blooms alter the

ecological balance of these systems and give an un-

pleasant taste and smell to the water, thereby elevating

treatment costs. However, the greatest problem stems

from the fact that some species produce toxins

(cyanotoxins) and can cause serious public health prob-

lems. These toxins can accumulate in the food chain and

produce different symptoms of intoxication.

Cylindrospermopsis raciborskii (Woloszynska) See-

nayya et Subba Raju (Ordem Nostocales) is one of the

most worrisome bloom-forming species in Brazil due to

its extremely invasive nature and increasing occurrence.

Initially classified as having pan-tropical distribution

[7], C. raciborskii was soon recorded in subtropical

environments in Africa and the Americas as well as in

246 M. do C. BITTENCOURT-OLIVEIRA ET AL.

temperate regions, where it occurs in shallow lakes (for

more details see [8]. Massive populations of C.

raciborskii in a public water supply reservoir are

worrisome due to their capacity to produce hepatotoxins

(cylindrospermopsin) and neurotoxins (saxitoxins) [9].

C. raciborskii has multiple adaptation strategies, such

as resistance to herbivory, tolerance to low light intensity,

ability to migrate in the water column due to aerotopes,

storage and use of intracellular reserves and the capabil-

ity of fixing atmospheric nitrogen [10]. Populations with

straight and coiled trichomes have been observed occur-

ring simultaneously in different proportions in Australia

[8,11,12] and northeastern Brazil [13,14]. Although mo-

lecular investigations reveal that the straight and coiled

morphotypes pertain to the same species [11,15], it is not

yet clear how these morphotypes behave in response to

environmental conditions such as light intensity and wa-

ter temperature. In recent decades, the frequent occur-

rence of C. raciborskii in reservoirs and small lakes has

been recorded in different states of Brazil, especially in

the northeastern region of the country [13,16-21].

In stratified lakes, populations may reach peak density

in the epilimnion. With the data available in the literature,

however, it is not possible to generalize on vertical

movements or depths with light intensities that are more

adequate to the growth of this species [22].

Considering the scarcity of studies on populations with

straight and coiled trichomes that occur simultaneously

in their natural environment as well as the need for in-

formation on the behavior of these populations in nature,

the aim of the present study was to determine the spatial

and seasonal dynamics of these C. raciborskii morpho-

types in relation to light intensity and temperature in the

water column of a shallow eutrophic tropical reservoir.

2. Materials and Methods

2.1. Study Site

The Mundaú reservoir is located in the city of Garanhuns

(8°55′40″S to (8°57′04″S and 36°30′40″W to

36°29′02″W) 716 m above sea level in the state of Per-

nambuco (northeastern Brazil) (Figure 1). The reservoir

has a water accumulation capacity of approximately

1 968 600 m3, surface are of 4 km2 and mean deepness

around 11m. Its main purpose is to supply the public

drinking water, but it receives part the residential sewage

of the city [23]. The reservoir has pH ranging from alka-

line to neutral, with a high availability of phosphorus and

limited nitrogen [24]. The geographical region is

characterized by high temperatures and dry periods,

especially between October and March (summer); the

winter (April to September) is characterized by greater

precipitation and milder temperatures.

2.2. Site and Periods of Samplings and

Community Study ′

Spatial and seasonal variations in the population density

of the straight and coiled C. raciborskii morphotypes

were determined from collections made at a single

sampling site located near the central pelagic region of

the reservoir (8°56′40″S and 36°29′26.2″W) at six

sampling depths (surface, 0.5 m, 1.0 m, 2.0 m, 5.0 m

and 10.0 m) during the dry (October,06 and November,

06/2004) and rainy seasons (August, 17 and September,

21/2004; June, 07 and August, 20/2005), only one

sampling for each month. Maximal depth at this site

varied according to the season (dry-10 m or rainy-12 m),

with a mean of 11 m during our study.

Throughout the water column, samples were

collected with a van Dorn bottle and subsequently fixed

in 5% acetic Lugol solution for quantitative analysis.

Trichome counts were performed directly with the use

of a Fuchs-Rosenthal chamber and a binocular optical

microscope (Nikon, Japan). Whenever possible, a

minimal number of 450 trichomes were counted for

each morphotype in order to obtain a 5% error and 95%

level of confidence [25]. Morphological analysis

involved measurements of the length and width of the

vegetative cells (n = 1 800), heterocysts (n = 450) and

number of cells per trichome (n = 600) in both morp-

hotypes, with the aid of a micrometered ocular coupled

to the microscope.

2.3. Abiotic Analyses

Air temperature was measured with a common mercure

thermometer and water temperature was obtained using

an YSI field probe (model 556). Depth (m) was

determined with a bathymeter (Garmin, Fishfinder 100).

Light intensity was accessed using a photometer (LI-

COR, model LI-250) with an underwater cable and

spherical sensor. Precipitation during the sampling

months was obtained from the National Meteorology

Institute in the city of Caruaru [26].

2.4. Statistical Methods

The normality of the data was tested for the choice of

analyses of variance and correlation. Analysis of vari-

ance (ANOVA, 5% level of significance) was used with

normal data to determine the occurrence of seasonal and

vertical variations. Spearman’s correlation coefficient

M. do C. BITTENCOURT-OLIVEIRA ET AL. 247

Figure 1. Map of study area; Mundaú reser voir, PE, nor theastern Brazil.

36º29'02"W

36º30'40"W

08º55'40"S

Mundaú reservoir

Sampling satation

500 m

08º57'04"S

(rs) was used to determine associations between abiotic

variables and morphotype density. Tukey test was used

to analyze temporal differences. The Statistica 2004 pro-

gram (StatSoft, Inc., Tulsa, OK, USA) was employed for

all analyses.

3. Results

During the study period, mean monthly air temperature

ranged from 21.6 to 23.1℃ in the rainy season and from

23.1 to 29.1℃ in the dry season. Figures 2 and 3 display

underwater light intensity, water temperature, straight

and coiled trichome density and precipitation.

Water temperature exhibited significant seasonal

differences (F = 20 832, p < 0.001). October/04 and

November/04, months of dry season, show statistical

differences of rainy months (Tukey, p < 0.05). The water

column was uniformity in October and November 2004,

in these months no significant difference was found for

light intensity (Figures 3(a), (b)).

During the months sampled, single-species blooms of

C. raciborskii (straight and coiled morphotypes) comp

osed the entire phytoplankton community, which is

common in this body of water.

Both morphotypes exhibited seasonal and vertical

differences in density (Fstraight = 5.232; Fcoiled = 10.894,

p < 0.001 and Fstraight = 5.579; Fcoiled = 9.913, p < 0.001,

respectively). Greater densities occurred in the rainy

season (5.3 and 4.3 x 107 trichomes mL−1 or 2.7 and 2.4

× 109 cell mL−1 for straight and spiraled morphotypes,

respectively, data not shown). There was a predomina-

nce of straight trichomes when light intensity was above

8 µmol m−2·s−1 and temperature was above 24℃. The

coiled morphotype had greater densities in this same

light intensity range but with the temperature below 24

ºC. There was a tendency toward the predominance

248 M. do C. BITTENCOURT-OLIVEIRA ET AL.

b c d

Deth (m)

0.0

0.5

1.0

2.0

5.0

10.0

(106 trichomes. mL–1)

Density

(106 trichomes. mL–1)

Density

90 mm*

0.0

0.5

1.0

2.0

5.0

10.0

Deth (m)

(106 trichomes. mL–1)

Density

140 mm*

0.0

0.5

1.0

2.0

5.0

10.0

Deth (m)

320 mm*

Deth (m)

0.0

0.5

1.0

2.0

5.0

10.0

(106 trichomes. mL–1)

Density

110 mm*

21 22 23 24 25 26 27 28 2921 22 23 24 25 26 27 28 29

0 20 40 60 80 100

Water temperature (℃)

21 22 23 24 25 26 27 28 29

Water temperature (℃)Water temperature (℃)

Water temperature (℃)

21 22 23 24 25 26 27 28 29

Water temperature

Light intensity

Straight morphotype

Coiled morphotype

(μmol photons.m–2, s–1)

Light intensity

0 20 40 60 80 100

(μmol photons.m–2, s–1)

Light intensity

0 20 40 60 80 100

(μmol photons.m–2, s–1)

Light intensity

(μmol photons.m–2, s–1)

a Light intensity

0 20 40 60 80 100

Figure 2. Vertical variation in trichome density of straight and coiled C. raciborskii morphotypes in relation to water

temperature and underwater light intensity at the Mundaú reservoir in the rainy season; (a) August, 17/2004; (b) Septe mber,

21/2004; (c) June,07/2005; (d) August, 20/2005; * accumulated monthly rainfall.

Density

(106 trichomes. mL–1) (106 trichomes. mL–1)

Density

60 0

1020

3040

Deth (m)

10.0

5.0

2.0

1.0

0.5

Deth (m)

10.0

5.0

2.0

1.0

0.5

0.0

21 2223242526272829

2627 28 29

Water temperature (℃) Water temperature (℃)

b a

(μmol photons.m–2, s–1)

Light intensity

0 20 40 60 80 100

(μmol photons.m–2, s–1)

Light intensity

0 20 40 60 80 100

Water temperature

Light intensity

Straight morphotype

Coiled morphotype

7 mm*

5 mm*

Figure 3. Vertical variation in trichome density of straight and coiled C. raciborskii morphotypes in relation to water

temperature and underwater light intensity at the Mundaú reservoir in the dry season (a) October, 06/2004; (b) November,

06/2004; * accumulated monthly rainfall.

M. do C. BITTENCOURT-OLIVEIRA ET AL 249

Figure 4. Variation in vegetative cell size, mean and standard deviation values for straight and coiled Cylindrospermopsis

raciborskii morphotypes during rainy and dry season (a. length, b. width).

of coiled trichomes when light intensity was below 3

µmol m−2·s−1. The straight morphotype exhibited a

greater number of trichomes with heterocysts in

comparison to the coiled morphotype, which were only

found in October and November 2004 (dry season) and

in September 2004 (rainy season)( data not shown).

An analysis of the data on C. raciborskii between

different sampling depths and months reveals that the

densities of both morphotypes had a positive correlation

with light intensity (rsstraight = 0.372 and rscoiled = 0.399, p

< 0.001). Both morphotypes also had a negative

correlation with depth (rsstraight = − 0.486 and rscoiled = −

0.557, p < 0.001) .

The Mundaú reservoir was stratified in the dry season,

with higher temperatures and greater light intensity in the

surface layers (down to 1 m) and a predominance of the

straight morphotype. In the lower strata, the coiled mor-

photype exhibited greater densities, but with no signifi-

cant differences. The straight morphotype population

was tolerated to high light intensity (83.23 to 92.26

µmol m−2·s−1) and temperatures (25.5 to 28.0℃),

whereas the coiled morphotype was proved as more

susceptible to light intensity. The existence of strata with

different water densities may facilitate the permanence of

the coiled morphotype population in the lower layers of

the water column, which is more adequate to its

development.

In the rainy season (winter), the reservoir remained

shallow (10 to 12 m), with evident thermal de-

stratification. Variations in temperature were lesser than

those found in the summer months and there was low

light intensity throughout the water column, with an

extreme reduction in light below the surface layers. The

general pattern of the populations under these cond-

itions was a predominance of the coiled morphotype at

higher depths (to 1 m), with the exception of September

2004, and there was a balance between the morphotypes

at greater depths, with a slight predominance alternating

between the two morphotypes. The coiled morphotype

population developed well under conditions of low light

intensity and milder temperatures, which are character-

istics commonly found in the winter months.

The mean length and width of the vegetative cells

were similar in both morphotypes, regardless of the

season and with no differences beyond the shape of the

trichome. In the straight morphotype, vegetative cells

measured 6.14 to 6.92 µm in length and 2.68 to 3.03 µm

in width. In the coiled morphotype, vegetative cells

measured 6.46 to 7.03 µm in length and 2.68 to 3.12 µm

in width (Figure 4). In straight morphotype the

heterocysts measured 6.73 to 7.09 µm in length and

2.79 to 3.01 µm in width; the number of cells per

trichome was 47 to 56 and in the coiled morphotype the

heterocysts measured 6.79 to 7.02 µm in length and

2.84 to 3.02 µm in width and the number of cells per

trichome was 49 to 59.

4. Discussion

According to [27], populations of cyanobacteria exhibit

considerable growth under conditions of high tempera-

ture, low N:P ratio and alkaline pH. However, the

dominance of one species or another depends on its

particular characteristics, survival strategy, nutritional

250 M. do C. BITTENCOURT-OLIVEIRA ET AL.

requirements and need for light. During the study period,

the Mundaú reservoir exhibited environmental character-

istics that allowed the occurrence of high densities of C.

raciborskii, such as high concentrations of phosphorus,

high temperature (above 21℃) and availability of light in

the epilimnion, but with an accentuated drop in the

metalimnion and hypolimnion.

In northeastern Brazil, the summer months are

characterized by low rainfall and high temperatures,

whereas rains occur during the winter months,

accompanied by a slight drop in temperature and lesser

light intensity. The highest density values were reached

in the rainy season due to the increase in the

concentration of nutrients carried by the rain as well as

the circulation of the mass of water, which stirs up the

sediment and suspends nutrients in the water column.

Among the rainy months, September had the greatest

densities of both the coiled and straight C. raciborskii

morphotypes. This was perhaps due to the higher

temperatures (22.8 to 24.1℃) in comparison to other

months in the rainy season. However, there was a more

uniform distribution of the C. raciborskii populations at

the different depths in the other months of this season

(August 2004; August and July 2005); at a depth of 10

meters trichome density was more than double that found

in September 2004. This difference at greater depths in

this month as well as the concentration of populations in

more surface layers (0 to 2 meters) may have been

influenced by the tendency toward stratification that

occurred in September.

According to [11], there is a clear difference in growth

rate between the two C. raciborskii morphotypes in

response to variations in temperature and light intensity.

The coiled morphotype tends to grow more quickly

under different environmental conditions than the

straight form due to its tolerance to high temperature and

low light intensity. It is believed to favor the dominance

of the coiled over the straight morphotype in tropical

ecosystems. However, the results observed in the

Mundaú reservoir contradict these findings. On the other

hand, the results are in agreement with a study by [28],

who compared the growth of the straight and coiled C.

raciborskii morphotypes under controlled light and

temperature conditions; the straight morphotype was

more tolerant to higher luminosity and temperature,

which led to faster growth rates, whereas the coiled

morphotype always exhibited slower growth, even at

lower temperatures and lesser luminosity; at high

temperatures and luminosity, the coiled population did

not develop well.

No akinetes were found in any other months sampled,

even when there were variations in temperature between

the rainy and dry seasons. In a shallow lake in France,

[29] found that the occurrence of C. raciborski blooms

depended mainly on climatic factors such as air tem-

perature, water temperature and light intensity. This

confirms the observations made by [30] that

temperatures between 22 ℃and 23.5℃ favor the

germination of akinetes. The lack of akinetes in the

present study suggests the occurrence of factors

favorable to the maintenance of the trichomes

throughout the entire study period, as these cells

develop under adverse environmental conditions.

Monitoring a small, shallow reservoir (Solomon Dam,

Australia), [31] found that stable stratification

conditions during dry periods were favorable to the

expansion of C. raciborskii populations. In the Mundaú

reservoir, the uniformity in the temperature of the water

column and low luminosity associated to the drowning

effect promoted greater population development when

compared to months in which thermal stratification

occurred. Thermal de-stratification in the rainy season

favored the increase in the populations of both C.

raciborskii morphotypes by providing more adequate

conditions for their growth, namely, lesser light

intensity and milder temperatures, which are

characteristics of the winter months in the hinterland

region of the state of Pernambuco in northeastern Brazil.

The species Cylindrospermopsis raciborskii persisted

under a variety of temperature and light conditions,

demonstrating adaptability to environmental variables,

which has also been reported for other regions in the

world. Due to the potential toxicity stemming from the

occurrence of high densities of this species, there is an

accentuated need for monitoring water quality in this

reservoir.

5. Acknowledgements

This study was supported by grants from CNPq

(Brazilian Council for Research and Development-

MCBO: 300794/2004-5) and FAPESP (State of São

Paulo Research Foundation – MCBO: 2006/03878-6).

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