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Perspectives on the Use of Algae as Biological Indicators for Monitoring and


Protecting Aquatic Environments, with Special Reference to Malaysian
Freshwater Ecosystems

Article · December 2010

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Tropical Life Sciences Research, 21(2), 63–79, 2010

Perspectives on the Use of Algae as Biological Indicators for Monitoring and


Protecting Aquatic Environments, with Special Reference to Malaysian
Freshwater Ecosystems

Wan Maznah Wan Omar *

School of Biological Sciences, Universiti Sains Malaysia, 11800 USM, Pulau Pinang, Malaysia
Centre for Marine Coastal Studies (CEMACS), Universiti Sains Malaysia, 11800 USM,
Pulau Pinang, Malaysia

Abstrak: Komuniti alga mempunyai banyak sifat-sifat sebagai penunjuk biologi perubahan
ruang dan masa alam sekitar. Parameter alga, terutamanya struktur komuniti dan variabel
berfungsi yang dapat digunakan dalam program pemantauan biologi dibangkitkan dalam
dokumen ini. Penunjuk biologi seperti alga hanya sejak kebelakangan ini dimasukkan ke dalam
penilaian kualiti air di beberapa kawasan di Malaysia. Penggunaan parameter alga untuk
mengenal pasti pelbagai bentuk pendegradan air adalah perlu dan pelengkap kepada
penunjuk alam sekitar yang lain.

Kata kunci: Pencemaran Air, Alga, Diatom, Pemantauan Biologi, Penunjuk Biologi

Abstract: Algal communities possess many attributes as biological indicators of spatial and
temporal environmental changes. Algal parameters, especially the community structural and
functional variables that have been used in biological monitoring programs, are highlighted in
this document. Biological indicators like algae have only recently been included in water quality
assessments in some areas of Malaysia. The use of algal parameters in identifying various
types of water degradation is essential and complementary to other environmental indicators.

Keywords: Water Pollution, Algae, Diatom, Biological Monitoring, Biological Indicators

INTRODUCTION

Governmental agencies and the general public have become increasingly concerned
about maintaining the quality of aquatic resources. Physical and chemical
measurements provide quantitative data on the presence and levels of aquatic
pollution and degradation, but these parameters do not reflect the extent of
environmental stress reaching the living organisms or the subsequent effects of this
stress. Karr and Chu (1999) stated that our ability to protect biological resources
depends on our ability to identify and predict the effects of human actions on
biological systems; thus, the data provided by indicator organisms can be used to
estimate the degree of environmental impact and its potential danger for other living
organisms. Kovacs (1992) defined biological indicators as organisms (or populations)
whose occurrence reflects the environmental conditions. Biological monitoring is the
specific application of biological response for the evaluation of environmental change
for the purpose of using this information in quality control program. In an effort to
characterise more precisely the cumulative impact of human activities on

*
Corresponding author: [email protected]
63
Wan Maznah Wan Omar

ecosystems, it is important to shift environmental monitoring from sole reliance on


chemical indicators towards the increased use of biological conditions (McCormick &
Cairns 1994).
Algae are an ecologically important group in most aquatic ecosystems and
have been an important component of biological monitoring programs. Algae are
ideally suited for water quality assessment because they have rapid reproduction
rates and very short life cycles, making them valuable indicators of short-term
impacts. Algal assemblages are typically species rich, and algal species exhibit wider
distributions among ecosystems and geographical regions. As primary producers,
algae are most directly affected by physical and chemical factors. Algal assemblages
are sensitive to some pollutants and they readily accumulate pollutants, and algal
metabolism is also sensitive to the variation of environmental and natural
disturbances. Algae are easily cultured in the laboratory and sampling is easy,
inexpensive and creates minimal impact on resident biota; relatively standard
methods exist for the evaluation of functional and non-taxonomic structural
characteristics of algal communities (Stevenson & Lowe 1986; Rott 1991; Round
1991; Van Dam et al. 1994; McCormick & Cairns 1994; Stevenson & Pan 1999).
Alterations and shifts in the species composition and productivity of algal
assemblages in response to anthropogenic stresses should be considered in order to
predict the effects on food web interactions and other ecosystem components
(McCormick & Cairns 1994). Algae affect the taste and smell of water, and
forecasting the movement and growth of algae in river systems is important for
operational managers responsible for the distribution and supply of potable water
(Whitehead & Hornberger 1984).
Periphyton are one of the most important algae associated with substrates in
aquatic habitats. Periphyton have been widely used as a tool for biologically
monitoring water quality (e.g., Leland & Carter 1985; Newman et al. 1985; Cosgrovea
et al. 2004). These organisms exhibit high diversity and are a major component in
energy flow and nutrient cycling in aquatic ecosystems. Many characteristics of
periphyton community structure and function can be used to develop indicators of
ecological conditions in the aquatic ecosystem (Hill et al. 1999). Periphyton are
sensitive to many environmental conditions, which can be detected by changes in
species composition, cell density, ash free dry mass (AFDM), chlorophyll, and
enzyme activity (e.g., alkaline and acid phosphatase). Each of these characteristics
may be used, singly or in aggregation, to assess conditions with respect to societal
values, such as biological integrity and trophic condition. The advantages that
periphyton communities have over other organisms for monitoring purposes include
the following: fixed habitats, so they cannot avoid pollution; relatively quick
recolonisation after perturbations in water quality or flow, the ability to enable a rapid
resumption of monitoring; the ease of sample preparation for analysis; and
widespread, common taxa, enabling their pollution tolerances to become well known
(Biggs 1985).

64
Algae as Biological Indicators

Diatoms have been used extensively in water quality monitoring (Round


1991). They exist in a wide range of ecological conditions, colonising almost all
suitable habitats; they can thus provide multiple indicators of environmental change
(Stevenson & Bahls 1999). Indices of water quality using diatoms gave the most
precise data compared to chemical and zoological assessment (Leclercq 1988).

Algae as Bioindicators of Aquatic Ecosystem Health

Aquatic populations are impacted by anthropogenic stress, resulting in a variety of


alterations in the biological integrity of aquatic systems. Algae can serve as an
indicator of the degree of deterioration of water quality, and many algal indicators
have been used to assess environmental status. Kolkwitz and Marsson (1908) were
the pioneers who classified algal species based on their tolerance to various kinds of
pollution. They stated that the presence of certain species of algae could define
various zones of degradation in a river. Palmer (1969) published a composite rating
of algal species that could be used to indicate clean and polluted waters. Patrick
(1949) developed community indices and provided information that demonstrated that
a healthy community is made up of numerous species in several groups of
organisms, including algae. Patrick (1971) proposed a numerical approach to study
water quality using diatom flora attached to glass slides as artificial substrates. Dixit
et al. (1992) discussed diatom flora as a powerful indicator of environmental change
and its emergence as a preferred indicator in monitoring studies. Algae are also used
in laboratory bioassays to study water quality, using media for culturing indicator
species from the field or defined media to which varying degrees or concentrations of
the pollutant are added (Ho 1980; Guckert et al. 1992; Grimshaw et al. 1993; Knauer
et al. 1997). Table 1 summarises the algal attributes and indicators that were used in
biological monitoring programs. To define the effects of various types of river
degradation, it is important to use a variety of algal parameters (Patrick 1973).
Nutrient enrichment is one of the most common anthropogenic stresses in
lakes, and limnologists have demonstrated the strong relationship between nutrient
loading and phytoplankton biomass. Algae can grow in abundance to the extent that
they change the colour of water, which can significantly impair the recreational uses
of aquatic systems. Blue-green algal toxins are contained within the living cells and
will be released by cell decay. Eutrophication is a fundamental concern in the
management of all water bodies and has been one of the focal points of
contemporary research in lakes, leading to the development of several statistical
models to predict the effects of nutrient loading on phytoplankton biomass. Blue-
green algal blooms are an environmental hazard that impairs the quality of water in
lakes, reservoirs and rivers. Predictive models based on the microbial and ecological
processes in freshwater bodies are useful for developing management responses
aimed at reducing the negative consequences of algal blooms on the community.

65
Wan Maznah Wan Omar

Table 1: Main algal attributes and associated indicators commonly used in monitoring
programs (modification from McCormick & Cairns 1994).
Attribute Indicator Reference
Community structure
Biomass Ash-free-dry-weight (AFDW) Ho* (1976); Vymazal and
Richardson (1995); Putz (1997);
McCormick et al. (1997); Hill et al.
(2000a)
Chlorophyll a Ho* (1976); Joy et al. (1990);
Welch et al. (1992); Putz (1997);
Hill et al. (2000a); Biggs (2000)
Autotrophic index (AFDW: Putz (1997); Bourassa and
chlorophyll a) Cattaneo (1998); Wan Maznah et
al.* (2000); Hazzeman* (2008)
Cell biovolume Stevenson and Lowe (1986)
Diversity Species diversity (diatom) Stevenson (1984); Nather Khan*
(1991); Ho and Peng* (1997);
Stewart et al. (1999); Maznah and
Mansor* (1999); Wan Maznah and
Mansor* (2002); Hazzeman*
(2008)
Species richness Anton* (1981); Nather Khan*
(1990); Maznah and Mansor*
(1999)
Composition Multivariate analysis (diatom) Sabater et al. (1988); Kelly et al.
(1995); Stewart et al. (1999); Hill et
al. (2000a); Winter and Duthie
(2000); Wan Maznah and Mansor*
(2000, 2002); Nor Ashidi et al.*
(2006); Makhlough* (2007)
Similarity indices (diatom) Heckman et al. (1990); Stevenson
(1984); Maznah and Mansor*
(1999)
Community
metabolism Ho* (1976); Keithan and Lowe
Net production Change in biomass (1985); Biggs (2000)
Relative specific growth rate Rosenfeld and Roff (1991); Rier
and King (1996)
Productivity Oxygen evolution Tease et al. (1983); Blanck (1985)
Radioisotopic tracer (14C) Keithan & Lowe (1985);
Shamsudin* (1987); Napolitano et
al. (1994); Vadeboncouer & Lodge
(2000)
Photosynthetic capacity Napolitano et al. (1994); Rier and
King (1996)
Bioaccumulation Nutrients Grimshaw et al. (1993)
Metals Knauer et al. (1997); Paweena*
(2005)
(continued on next page)

66
Algae as Biological Indicators

Table 1: (continued)
Attribute Indicator Reference
Metabolic state Adenylate energy charge Hino (1988)
Biomolecules Ribonucleic acid Guckert et al. (1992); Napolitano
et al. (1994)
Enzyme activity Alkaline phosphatase activity Guckert et al. (1992)
Population analyses
Indicator species pH index Cox (1990); Whitmore (1989)
Pollution tolerance index Palmer (1969); Descy (1979);
Lange-Bertalot (1979); Kelly
et al. (1995)
Saprobien index Pantle and Buck (1955); Lange-
Bertalot (1979); Friedrich et al.
(1992); Ho and Peng* (1997);
Wan Maznah and Mansor*
(2002); Makhlough* (2007);
Hazzeman* (2008)
Diatom index Prygiel and Coste (1993); Kelly
et al. (1995)
Microalgae spectral analysis Vanlandingham (1976)
Trophic index Whitmore (1989); Makhlough*
(2007)
Growth Algal growth potential Ho* (1980); Pringle (1987);
Lukavsky (1992); Fujimoto and
Sudo (1997); Wan Maznah et
al.* (2007)
Note: * indicates research conducted in Malaysia

Running waters dominate the Malaysian inland aquatic environments and


support a rich diversity of flora and fauna (Khoo et al. 2003), whereas man-made
lakes dominate among the lentic ecosystems. In Malaysia, development has
inevitably resulted in adverse changes in the hydrology and ecology of wetland
ecosystems. The developments are associated with more land use, increases in
population urbanisation and industrialisation, and the expansion of irrigated
agriculture, all of which have affected the quantity and quality of the water supply
(Ho 1995; Sánchez et al. 2007). It was expected that Malaysia will face a water
shortage by 2010, when its existing water production capacities will be reduced due
to demands such as human population and economic growth (Chan & Nitivattananon
2006). The Department of Environment (DOE) has classified 40 rivers as polluted
and about half of that number is on the “most polluted” list. In Malaysia, biological
aspects have only recently been included in the integrated water quality monitoring
program study, and few algal studies have been conducted in relation to water
pollution. Most of the information from water quality studies remains unpublished, and
some of it is available through regional seminars or internal university press.

67
Wan Maznah Wan Omar

One of the earliest algal studies conducted in relation to water pollution was
carried out by Ho (1976), who studied periphyton production in the disturbed
Renggam Stream, Selangor. Nather Khan (1985, 1990, 1991) conducted studies on
the pollution status of the Linggi River Basin, Seremban, Negeri Sembilan using
diatoms and reported that there was a marked variation in species between the
unpolluted and polluted stations. Anton (1981) recorded a decrease in periphytic algal
species in the downstream stations due to heavy siltation in the Langat River,
Selangor. Phytoplankton composition changed in response to the addition of both
NO3-N and PO4-P in the Ulu Langat Reservoir, Selangor (Anton & Abdullah 1982),
and Cyanophyta was dominant when nitrogen was the limiting factor. Mansor and
Lidun (1992) reported the presence of several species of filamentous algae and a
high nutrient concentration in the Pulau Pinang rivers, which strongly indicated that
some of them are polluted. Maznah and Mansor (1999) studied diatom diversity and
its relation to river pollution and concluded that diversity values could be related to
changes in water quality. In a related study, Wan Maznah and Mansor (2000)
reported the occurrence of clean, polluted and brackish diatom species collected from
artificial substrates (glass slides) along the Pinang River Basin, Pulau Pinang and its
tributaries (Table 2). The differences in the specific sensitivity of certain diatom
species to pollution were a reliable and useful means of assessing the degree of
pollution in the Pinang River system, but the diversity of diatoms could not be directly
related to water quality (Wan Maznah & Mansor 2002).

Table 2: Clean, polluted and brackish water species of diatoms attached to artificial substrates
(glass slides) at the Pinang River Basin (Wan Maznah & Mansor 2000).
Clean water species Polluted water species Brackish water species
Achnanthes minutissima Achnanthes exigua Cocconeis sp.
Achnanthes oblongela Achnanthes exigua var. Coscinodiscus argus
heterovalva
Achnanthes woltereckii Hantzschia amphioxys Coscinodiscus antiquus
Cocconeis placentula Nitzschia amphibia Coscinodiscus excentricus
Cocconeis pediculus Nitzschia fonticola Coscinodiscus decipiens
Cocconeis thumensis Nitzschia palea Coscinodiscus symmetricus
Eunotia pectinalis var. minor Pinnularia biceps Cyclotella comta
Fragilaria capucina Pinnularia biceps f. petersenii Cyclotella striata
Gomphonema acuminatum Pinnularia microstauron Diploneis ovalis
Psammothidium bioretii Diploneis interrupta
Surirella linearis Diploneis bombus
Surirella tenuissima Nitzschia littoralis
Nitzschia obtuse
Nitzschia obtuse var.
scalpelliformis
Nitzschia sigma
Surirella ovalis

68
Algae as Biological Indicators

Algal studies were also included in the river monitoring program by the
Department of Environment (DOE 1998, 1999) to indicate the trend and status of the
water quality of Malaysian river systems. Ho and Peng (1997) classified the water
quality of the Perlis River (Perlis), Perai River (Pulau Pinang) and Juru River (Kedah)
based on the abundance and species composition of phytoplankton. Yeng (2006)
reported that water pollution in the Ahning Reservoir, Kedah was associated with the
appearance of certain species of phytoplankton, especially dinoflagellates. Yap
(1997) used the Shannon index and the saprobic index of phytoplankton for water
quality assessment of a river ecosystem and concluded that ecological knowledge
can be used in the management of a water body. In Malaysia, the determination of
trophic state has been conducted primarily by measurements of physico-chemical
parameters, primary productivity and chlorophyll-a concentration. In a study
conducted in the Muda and Pedu Reservoirs, Kedah (Zulkifli 1980), it was found that
both reservoirs were slightly eutrophic based on the phytoplankton assemblages, with
moderate levels of nitrogen, alkalinity and pH. In another study conducted in the
Mengkuang Reservoir, Pulau Pinang (Makhlough 2007), Carlson modified the trophic
state index (Carlson 1977) and showed that the reservoir was near to a mesotrophic
state based on the chlorophyll-a and Secchi disk transparency data, but the Shannon
and saprobic indices of phytoplankton indicated that the reservoir was slightly
polluted (class III) and moderately polluted (class II), respectively. The study also
recorded the presence of Anabaena, Microcystis, Oscillatoria, Nostoc, Dinobryon,
Chroococcus, Staurastrum paradoxum and Mallomonas, which are indicators of
toxicity and pollution in aquatic ecosystems, thereby showing that algological studies
are important for water quality assessment and can provide an early warning sign of
water degradation.

Approaches for Biomonitoring of Aquatic Ecosystems Based on Algae

The oldest approach for using algae to assess stream water quality is based on the
indicator species concept (Saprobien system). The Saprobien system is widely used
in municipal and wastewater monitoring (Hill et al. 2000a) and discriminates between
polluted and clean streams (Ho & Peng 1997). In our monitoring study conducted at
the Pinang River Basin, Pulau Pinang (one of the polluted river basins in Malaysia),
the saprobic index (Pantle & Buck 1955), which was based on diatom species
assemblages on glass slides, successfully divided the sampling stations into four
zones of saprobic contamination: the Polysaprobic Zone, the Alpha-mesosaprobic
Zone, the Beta-mesosaprobic Zone and the Oligosaprobic Zone. The zones of
saprobic contamination were characterised by the occurrence of certain groups of
diatom species, namely Saprobiontic species, Saprophilic species, Saproxenous
species and Saprophobous species (Wan Maznah & Mansor 2002). The saprobic
index was calculated based on periphytic algal species composition in the Petani
River Basin, Kedah (Hazzeman 2008) and revealed that water quality evaluation
using diatom indices was consistent with the physical and chemical determination
(Lehmann & Lachavanne 1999; Almeida 2001). Chemical stresses in aquatic
ecosystems modify the taxonomic composition of the algal population, causing a

69
Wan Maznah Wan Omar

reduction of sensitive species and an increase in the number of tolerant species


(Genter & Lehman 2000; Biosson & Perrodin 2006).
A hierarchical framework is being used in the development of the periphyton
indices of aquatic ecosystems. The framework involves the calculation of composite
indices for biotic integrity, ecological sustainability, and trophic condition. The
composite indices are calculated from the measured or derived first-order and
second-order indices. The first-order indices include species composition (richness,
diversity) (e.g., Winter & Duthie 2000; Soininen & Niemelä 2002; Potapova et al.
2005; Yallop et al. 2009), cell density, AFDW, chlorophyll, and enzyme activity (e.g.,
Saylor et al. 1979), which individually are indicators of the ecological conditions in an
aquatic ecosystem. Second-order indices are calculated from periphyton
characteristics, such as the autotrophic index (Weber 1973) and community similarity,
compared to reference sites. Irvine and Murphy (2009) used a ‘weight of evidence’
approach to assess the trophic status and phytoplankton community characteristics in
the Buffalo River, USA Area of Concern (AOC). They found that the phytoplankton
community exhibits some anthropogenic impact, but that these impacts do not
indicate extreme stress.
The approach based on the algal indices of community structure (diversity,
evenness, richness, similarity), with the assumption that a pristine and healthy
environment is typified by a greater diversity of organisms than found in degraded
environments, has been used for monitoring rivers. However, several studies have
questioned its reliability (Archibald 1972; Descy 1979; Stevenson 1984; Nather Khan
1991; Ho & Peng 1997; Maznah & Mansor 1999), arguing that the relationship
between diversity and environmental quality is more complex than was previously
thought and that the diversity might be high in stressed environments. Although the
study conducted at the Pinang River Basin demonstrated that the difference in diatom
species diversity could be related to changes in water quality (Wan Maznah &
Mansor 2002), comparing diversity as a tool to discriminate water quality conditions
was restricted to sampling stations upstream from those near the estuary. To
accurately estimate the water quality using species diversity, it is necessary to
precisely define the species that compose the community and to have thorough
knowledge of their autecology (Archibald 1972).
Multivariate analysis that is based on the correlation of organism
assemblages (especially diatoms) with environmental data has been developed to
assess water quality (Sabater et al. 1988; Kelly et al. 1995; Hill et al. 2000a; Winter &
Duthie 2000). Researchers found that the methods that compare the distribution
patterns of diatom communities in the rivers with physico-chemical parameters allow
for the analysis of the relationship between biotic and abiotic variables. Discriminant
analysis using the density of diatoms attached on glass slides from our observation at
the Pinang River Basin successfully discriminated sampling stations into clean,
polluted and brackish waters (Wan Maznah & Mansor 2002).
Non-taxonomic measures of algae (e.g., wet, dry and ash-free weights,
caloric contents, chlorophyll a and other photosynthetic pigments, and biochemical
components such as ATP and DNA) can also be useful for detecting effects not
indicated by taxonomic analysis (Hill et al. 2000b; Yamada & Nakamura 2002;
Cosgrovea et al. 2004). Periphytic algae fatty-acid biomarkers revealed differences in
the taxonomic composition of periphyton between reference and polluted sites
70
Algae as Biological Indicators

(Napolitano et al. 1994). Estimates of community biomass based on the AFDW and
chlorophyll a have been an integral part of ecological studies of aufwuchs concerning
production (as biomass accumulation overtime) (Ho 1976), both as a productivity
indicator or index of the photosynthetic potential and as an indicator of nutrient stress
or community conditions (Clark et al. 1979). Autotrophic index (AI), determined as the
ratio of AFDW:chlorophyll a in the periphyton collected on an artificial substrate,
indicates the degree of organically polluted waters. AI increases in proportion to the
concentration of organic matter (or BOD) because heterotrophs occupy a greater
portion of the biomass as organic pollutants increase (Welch & Lindell 1992). In the
study conducted at the Pinang River Basin (Wan Maznah et al. 2000) and Petani
River Basin (Hazzeman 2008), AI reflects the conditions of the sampling stations,
which have different levels of pollution; the results were consistent with those
reported by Weber (1973), Clark et al. (1979), Matthews et al. (1982), Bourassa and
Cattaneo (1998) and Hill et al. (2000b).
The problems associated with blue-green and toxic algae have prompted
long-term monitoring of the physical, chemical and biological parameters of
freshwater ecosystems worldwide. Data from these monitoring activities contain a
wealth of information about the behaviour of these ecosystems that is rarely fully
explored.

Concluding Remarks

There is a great variety of methods by which algae may be used as indicators of river
water quality. Although the biotic indices and non-taxonomic measurements of algae
clearly reflect the conditions of water quality, it is important to note that such
measurements should not be taken as an absolute measure of the river perturbations
but may be considered as a helpful description of the algal community response to
such disturbances that complements other environmental indicators. Because no one
group of organisms is always best suited for detecting and assessing the
environmental disturbance associated with human activities, indicators derived from
several groups of organisms should be included in water quality monitoring programs
to provide a comprehensive signal of ecosystem change.

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