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Mitigation and Adaptation Strategies for Global Change (2005) 10: 127143


Springer 2005


Canakkale Onsekiz Mart University, SUF, Department of Fisheries, 17100 Canakkale, Turkey
( Author for correspondence: Tel.: + 90-286-2180018 Ext. 1684; Fax: + 90-286-2180543;
E-mail: akarafistan@comu.edu.tr)

(Received 7 May 2003; accepted in final form 11 December 2003)

Abstract. Manyas, also known as the Bird Paradise Lake, is situated near the south-eastern coasts
of the Marmara Sea in Turkey. This shallow lake, is a unique natural reserve providing habitat for
migratory birds with its rich fauna and plankton species. The objective of this work is to study the
ecological and water quality changes resulting from increasing anthropogenic pollution and human
intervention on the natural variations of the water level. For this purpose, physical, chemical and
microbiological aspects of the aquatic ecosystem in the lake of Manyas are being measured semimonthly since more than a year. After the completion of field measurements associations between
different parameters will be searched by means of a water quality model. Results obtained will
be used in the sustainable restoration of the lake. In this paper, firstly the nutrient and trophic
dynamics of the planktonic ecosystem are associated with the bio-geochemical water cycle in the
lake. Secondly, space and time distributions of all physical, chemical and microbiological data are
presented and interactions between the nutrient availability and some microscopic communities are
Keywords: chemical and microbiological water quality, indicators, Manyas Lake, nutrient cycles,

1. Introduction
Manyas or Bird Lake (40 11 N, 27 58 E), is situated 14 km from the southeastern coasts of the Sea of Marmara, Turkey. Its origin is tectonic, related to the
well known seismicity of the Western Anatolian Fault (Leroy et al. 2002). Manyas
is a shallow eutrophic lake with many interesting properties. It receives fresh water
from several streams and underground as well. The lake water is always turbid,
because of its colloidal and clay content. Water level fluctuates naturally with
seasons, reaching the highest level of 6m in spring and the lowest level varying
between 12 m in summer.
Prof. C. Kosswig was the first to discover in 1938 that the lake lies on an important world wide migratory water bird route. The lake is rich in deep fauna and
plankton. There is also considerable amount of birds fertilizers. All these factors
contribute to diverse and intensive fish and bird populations, to sustain their lives.
The north-eastern part, covering 64 ha consists of woods where more than 266
bird species have been recorded to nest and more than 90 to breed. This area is



Figure 1. Localization of the sampling stations at Lake Manyas.

protected since 1959 as the first natural reserve area of Turkey. In 1976 the site was
granted a class A Diploma by the Council of Europe, recognizing the wetland to
be under protection as habitat for birds and also as a natural reserve. This special
status has subsequently been renewed four times (most recently in 1996). Also
in 1977 the entire lake was declared as a Permanent Wildlife Reserve, under the
protection of the Cultural and Natural Assets Law. In 1994 the eastern part of the
lake, covering 10,200 ha, was listed in the Ramsar Convention, with the same status
being extended to the whole lake in 1998. The site is managed by the Ministries
of Environment, Forest, Culture, Energy and Natural Resources. The park consists
of partially flooded forests which are mainly meadows and willows. There is an
observation tower and a visitors centre in the park.
Thus, Lake Manyas has been known to be one of the most important world
wide natural reserve for migratory birds and wild fowl species. The site holds
significant breeding populations of herons (e.g. Night Heron, and Grey Heron).
The lake is also an important reproduction area for the Dalmatian Pelican, as well
as Spoonbill and the Pygmy Cormorant liable to global extinction. Large numbers
of other cormorants (about 2000 pairs), White Pelican, White Stork, Red-footed
Falcon, geese, swans, ducks, terns and pink flamencos are passage birds observed
in the area. Oxyura leucocephala has been regularly recorded in winter. The site,



since its discovery as a bird sanctuary, is called Kus Cenneti which means Bird
Paradise. The lake was once used to support 23 fish species, as well as crayfish,
salamanders, turtles, water snakes and frogs. Further Kus Gl (Figure 1) is important for commercial fishery, mainly Cyprinus carpio. According to archaeologists
and historians (Bakir 1997) in the ancient history of Greece Xenophon describes
the lake as a very large wetland and associates Manyas to Paradise 4th century
B.C. (Leroy et al. 2002).
Around the lake, there are reed, rush and meadow areas. The main vegetation
seems to be at the limit of Mediterranean type with white willow as the most
common tree. The south and south-west shores of the lake are embanked and
the outflow is controlled by two regulators. During the summer months, when the
water level drops, the area becomes covered in lush vegetation. Some forests in the
southern part have given place to agricultural areas, lately. There are 14 villages
around the lake, with agriculture as main activity. Cattle and poultry farming are
also important sources of income. Ten villages discharge solid and liquid wastes
directly to the lake with no purification. Remaining 7 villages have biological
purification plants. Also among the 33 neighbouring factories only two posses
purification facilities. According to the environmental protection unit of the municipality, there exists totally 111 polluting point sources (poultry) discharging
directly to the streams with only 11 in possession of biological purification means.
In addition, runoff from households and numerous farms are being carried directly
into the lake with no treatment. Intensive use of fertilizers in the nearby farmlands
are also being carried to the lake. In the north-eastern part, Sgrc Stream brings
chemical pollution from the nearby industrial city of Bandirma. Especially Boron
and other chemicals are being processed in these factories.
Runoff from numerous farms, animal processing plants, households and factories are being carried to the lake directly where current waste treatment facilities
have insufficient capacity. Under these conditions eutrophication is inevitable.
This is a well known consequence of nutrient (i.e. nitrate, phosphate and silicate)
enrichment of closed or semi-closed water bodies or seas, such as the Mediterranean (Karafistan et al. 1998 and 2002).
We know that untreated polluting sources of surface water are responsible for
waterborne bacterial diseases (e.g. cholera and typhoid). On the other hand, the
lake receives at all times and by natural means bacteria from soil, air and rivers
as well as dead plants and organic matter. Only a small amount of these bacteria
find favourable existence conditions and they usually constitute the natural flora of
water. We must also add to the natural micro flora the by-products of anthropogenic
activities present in sewage, organic matter wastes from animal plants (especially
poultry in that area) and factories. Microbiological, and hence hygienic, water
quality can be determined from the biologically degradable organic matter (OM).
Behaviour of the bacterial loop with respect to nutrients is more complex, however.
Our aim in this work was to determine interactions between the above different components of the aquatic ecosystem in Lake Manyas. These interactions are



influenced by both the physical, chemical and microbiological water quality of the
lake as described in the following sections.
2. Characteristics of Data
Fluctuations in the lacustrine properties of Lake Manyas, are quite interesting on
the geological scale as a tectonic place, as well as the seasonal one as a natural
reserve. In this work we have limited our analysis to the seasonal variability of
certain water quality indicators and parameters. The five sampling stations shown
in Figure 1 were selected in such a way to provide a good local representation
of each section. Sampling always started at Station 1 and the same trajectory was
followed on a fishing boat to the last Station 5. Special care was taken for not
disturbing birds nesting at the national park, located in the vicinity of Station 2.
The surveys were done semi-monthly usually, except for February 2003 which was
too cold for any measurement on the lake.
Physical, chemical and microbiological water quality indicators were selected with
respect to the following properties;
Physical: The physical water quality parameters that were considered in the
monitoring program were temperature, PH, Secchi transparency and depth. Temperature is indeed a fundamental factor for water quality, exerting a great influence
over the aquatic system. Factors such as reductions in water flow and waste discharges may have a negative affect on its natural seasonal variability. pH is a known
standard measure of acidity and alkalinity. It drives many chemical reactions in
living organisms, where a pH value of 7 represents a neutral condition. These
parameters were measured in situ together with depth and transparency.
Nutrients and Chemical parameters: Nutrients most responsible for water quality degradation via eutrophication are nitrogen, phosphorus and silica. They are
found in the aquatic environment as dissolved inorganic or organic forms. Since
phosphate (PO4 ), silica (SiO2 ) and nitrate (NO3 ) are the most limiting factors for
the phytoplankton growth, they are also considered as water quality indicators.
Another nutrient required for life, is the ammonia (NH3 ) molecule, which can be
highly toxic for the aquatic life above a certain concentration. It was therefore
included in the analysis. Besides nutrients, metals such as zinc (Zn), iron (Fe),
calcium (Ca), magnesium (Mg), silica (Si), copper (Cu) and manganese (Mn) may
naturally be present in the lake water, due to its tectonic origin. Their concentrations might as well be modified by anthropogenic activities. Specially Boron (B)
processing is the most important activity in that area. It was added to the above list
with nickel (Ni) as chemical indicators of water quality.



Biological parameters: They consisted of phytoplankton counted per liter, for

the most dominant species relevant to the lacustrine ecosystem. The phytoplankton
was divided into two groups with different nutritive needs: on the one hand Bacillariophyceae, large diatoms consuming silicate for their growth. Secondly, a group
comprising several smaller species such as Cyanophyceae, Chlorophyceae which
need phosphate or nitrate for their growth.
Microbiological: Certain bacteria enter waters through inadequately treated
sewage or runoff of OM from pastoral farm lands. Wild life living in and around
the lake are also an important contribution to the production of OM. It is well
known that bacteria and fungi are responsible for the degradation of OM, and for
this reason they are commonly used as microbiological indicators of water quality.
Faecal material is an indirect source of decomposed organic matter (DOM) as the
solids are solubilized during microbial degradation. In fact heterotrophic bacteria
are known to assimilate dissolved OM and N compounds, as ammonium necessary
for protein synthesis (Lacroix and Gregoire 2002). For this reason, some of these
bacteria are used as water quality indicators when there is not enough nitrogen in
the aquatic environment. Recognized bacterial indicators for assessing water quality are bacteria of the Enterobacteriaceae family defined as total coliform bacteria
and the Fecal coliform bacteria. The coliform bacteria are gram-negative rods, with
the faecal coliform bacteria usually, but not always, found in the faeces of warm
blooded animals: The presence of faecal coliform bacteria in water is indicative of
contamination by faecal material and considered indicative of health risk. Significance of coliform group density is established as an indication of the degree of
pollution and the sanitary quality of water. Recently, the use of Escherichia coli
suggested as most sensitive indicator of faecal pollution. In addition to the above
bacteria Enterococcus and Staphylococcus are also used as indicators of either
faecal or organic pollution. Other types of bacteria are Pseudomonas; known to
degrade nitrogen compounds. Lactobacillus are associated to carbon products and
fungi to organic matter. All these bacteria have also been included in the analysis as
indicators of water quality, even though the results are not presented in this work.
Especially Enterococcus and Staphylococcus are important indicators of the whole
aquatic ecosystem health, including fish and birds via the food web. Indeed both
Escherichia coli and Enterococci are good indicators of gastrointestinal diseases.
The presence of such bacteria indicates the possible presence of faecal material.
Therefore, indicator bacteria concentrations are also used to determine if the water
quality is adequate for recreation. They are sometimes combined with the Pseudomonas bacteria which are well associated with skin infections. For this reason, we
used Pseudomonas and enter bacteria as indicators of microbiological water quality
in this lake.



3. Method of Analysis
Physical parameters were measured directly at the water surface by conventional
methods (Wetzel and Likens 1995). Two liters of water was collected by a water
sampling bottle (Ninsin) at each station and carried to the laboratory (200 km)
away. Standard photometric (Palintest 7000) analysis was employed for chemical
concentration determinations. Nutrient concentration measurements were calibrated and found to be competitive with those obtained by the autoanalyzer
technique of the Institute of Marine Science, at Erdemli. For the microbiological
sampling, two replicate water samples were taken 10 cm below the surface, and
collected in 150 ml glass sample containers. Water samples were brought to the
laboratory in ice boxes and analysed within 24 hours.
Indicator bacteria were measured as a concentration, usually expressed as an
estimate of the number of individual organisms per ml of water. Water quality
managers are interested in both the concentration of single samples, and in the average concentration of a series of samples taken over a period of time (Baumgart
1993; Schulze 1996). Evaluation of heterotrophic bacteria was done by plating on
highly selective culture media. In our microbiological laboratory, 7 different types
of commercial Agar plates given in Table I, were used. Incubation conditions and
method used for each culture are explained in the references. Colonies formed
after the necessary incubation period were counted directly, and the logarithm of
the arithmetic means were used in the graphical presentations.
Annual variations of the 4 physical parameters are given in Figures 2 (ad). Distributions of phytoplankton associated with the nutrients are shown in Figures 3, 4.
In these figures we observe that the degree to which the phytoplankton growth is
limited by the nutrient availability is variable with respect to the local conditions.
Microbiological test results are presented through the Figures 5 to 6. They are also
compared with the availability of the nitrogenous products such as ammonium,
nitrate and nitrite. As expected heterotrophic activity of Pseudomonas and enter
bacteria, continue in winter when ammonium is at the highest level. In Figures
7 and 8 space and time variability of some chemical parameters are presented.
The last figures reveal that the instantaneous peaks observed in December, should
obviously be due to discharge from point sources. From these figures one easily
notices that, besides the natural variability, the water quality and attributes of this
site are fluctuating rapidly both in space and time.



Incubation conditions and nutritive plates used analysis of microorganisms in Lake

Micro organism

(Plate Count Agar)
(Crystal Violet Galle Glucose Agar)
(Pseudomonas-Aeromonas Agar)
(Baird Parker Agar)
(M.R.S. Agar, pH-5)
(Kanamycin Agar)
(Malt Extract Agar)

T( C)

Total aerobic bacteria



30 (anaerobe)







30 (anaerobe)





4. Results and Discussion

The annual mean surface water temperature of Lake Manyas is around 12.5 C
in accordance with the meteorological mean (Figure 2a). The highest temperature
of 25 C is reached in July-August, and the lowest value of 2 C was recorded in
pH > 7 in Figure 2b indicates alkaline conditions in the lake, which is quite
variable throughout the seasons. It reaches maximum values of 89.5 at some
places in June-July, and similar to temperature has its minimum in December at
all stations. We know that some biological processes may adversely be affected by
sudden pH changes, which in return deteriorates the whole water chemistry. From
Figure 2c we also notice that, even though the lake water is usually turbid, the
Secchi transparency reaches 1.75 meters in May at the central station, where total
depth is around 4 meters (Figure 2d).
Distributions of the most abundant diatom (Bacillariophyceae) are shown in
Figure 3. Two bloom periods are occurring in JuneJuly and in December, with
about the same intensity. As expected, the maximal diatom concentrations are
directly followed by the minima of silicate. Similarly, we observe in Figure 4
the seasonal distributions of the smaller surface phytoplankton populations as a



Figure 2. Seasonal distributions of physical parameters; a) pH, b) Temperature, c) Secchi depth, d)


function of nitrate or phosphate as growth limiting factors. Chlorophyceae seem

to have a major peak in the north-western Station 1, in May. The bloom period
for the same phytoplankton have shifted to June for the north-eastern Station 2
(Bird Paradise), where the maxima correspond directly to the minima of NO3 . A
secondary PO4 peak follows in winter, especially at Station 1. This may be due to
the fact that no small phytoplankton seem to be present at that time of the year. The



Figure 3. Distributions of diatom and silicate; a) Bacillariophyceae, b) SiO2 in Lake Manyas.

same type of correlation is observed for Cyanophyceae, mostly abundant at Station

1 in May, with a corresponding NO3 decline in June.
Pseudomonas bacteria are known to assimilate directly the nitrogen present in
ammonia. This is easily noticed in Figure 5 where a rapid decrease in Pseudomonas
bacteria in April 2003 is followed by an abruptly increasing peak in ammonia,
in May 2003. As shown in Figures 6, heterotrophic activity of some (e.g. enter
bacteria) are similar in behaviour, accept the central Station 3 where enter bacteria
concentrations in August are above the bathing limit of EU-regulations (EU 1995).
Again the decrease in ammonium concentrations follow the bacterial peaks rather
rapidly. On the other hand, exceedingly high concentrations of ammonia occurring
in spring at Station 5 should be due to the nearby organic poultry pollution which is
brought by streams. Nitrite concentrations are showing low fluctuations throughout
the year, and a direct correlation is difficult to establish at a first glance. Sulphate, which is also associated to the bacterial activities is very high in December
(Figure 8a). It seems also plausible that the microbial regeneration of N occurs
throughout the year and in winter it reaches its highest level.
Indeed, for drinking water no faecal coliform should be present and they are not
wanted in general in the marine and lacustrine waters used for various purposes



Figure 4. Small phytoplankton and nutrient dynamics; a) Chlorophyceae, b) Cyanophyceae, c) NO3 ,

d) PO4 .

(bathing, fishing, etc.). However, from the Figures 5 and 6, representing the most
abundant indicator bacteria, we observe a significant continuous presence. According to general water pollution regulations, water quality in all stations is of class
III or even IV at the Natural Park. Compared to the EU microbiological water
quality criteria (EU 1995), the Park receiving pollutants from the Sgrc Stream



Figure 5. Pseudomonas bacteria and nutrient distributions; a) Bacterial counts, b) NH3 , c) NO2 .

has the highest number of Fecal and total coliform bacteria. This is a confirmation
for class IV, as an extreme level of pollution in this site, serving as habitat to birds.
We intend to extend the microbiological water quality analysis to micro flora of
fish in the future, in order to establish the level of pollution at the last chain of the
food web.



Figure 6. Distributions of Enterobacteria and nutrients; a) Bacterial counts, b) NH3 , c) NO2 in Lake

Distributions of Ca, Mg, Fe, Ni concentrations are presented in Figures 7a to

7d. Those of SO4 , B, Cu, Zn follow in the last Figure 8. Accept for Ca and Mg,
which are naturally present in water (particularly at Station 4 with springs) abrupt
increases in the concentrations of Fe, Ni (Figures 7c, 7d) and that of SO4, B, Cu,
Zn (Figures 8a8d) are encountered in December 2002, at Stations 1 and 5. On
the other hand, in Stations 1, 5, 3 Ca increases (Figure 7a) in May 2002, and that
of Mg in March 2003 (Figure 7b) are observed. The fact that concentrations of


Figure 7. Distributions of parameters; a) Ca, b) Mg, c) Fe, d) Ni in Lake Manyas.




Figure 8. Distributions of parameters; a) SO4 , b) B, c) Cu, d) Zn in Lake Manyas.



these elements show such instantaneous peaks, at Stations 1, 5, must be due to

discharge from numerous surrounding factories without purification. For example,
one of the largest borax and boric acid production industries in that region (Etibor)
has been estimated to discharge wastes about 6300 m3 /day. Sgrc Stream, itself,
is probably feeding the Park with 1700 m3 d1 of B products it is receiving from
this factory. From Figure 8b boron is seen to have two principal peaks, one in May
2002 and another the following December. Boron is also known to be limiting plant
growth and the degree of B pollution may create serious problems for the trees and
vegetation in that area.

5. Conclusions
It is, indeed difficult to judge about the degree of long term pollution and water
quality from short period measurements. The results presented in this work are
based only on observational analysis of one year measurements. It is evident even
from this picture alone that, Lake Manyas is facing many adverse factors in terms
of the quality and quantity of water it is receiving. The lakes water which was
potable in 1960s, has been observed to deteriorate in quality very rapidly the last
decades by many researchers, because of the anthropogenic activities. Also due to
over fishing, and the artificial water regime, fish and bird populations have been
declining considerably the last years. It is well known that natural water level
fluctuations are vital for the aquatic ecosystem health from the microscopic to
the macroscopic trophic level, since all are related by the aquatic food chain. It
seems, however, that the water level has been kept relatively high in recent years
for making use of the lake as a reservoir for irrigation. The forest not being subject
to any management scheme neither, feeding marshes and nesting trees for birds are
lost in some areas due to prolonged inundation.
In this study, it was demonstrated that Lake Manyas as a natural reserve, is
threatened by all types of anthropogenic pollution which have the impact and potential to alter the productivity of the whole ecosystem, via the food chain. Thus,
any perturbation in the chain may also alter the water quality besides the quantity.
As an example, nutrients such as N, P, and Si, which are most often responsible
for water quality degradation and eutrophication were considered. Their seasonal
variability were studied at 5 selected important spots. As a consequence, it was
found that the degree to which the phytoplankton growth is limited by this nutrient
load alone, depends on the local conditions and also varies with its availability
on the seasonal scale. Certain diatoms were observed to be abundant with two
bloom periods which corresponded to silicate minima. For the smaller phytoplankton species, a late spring or early summer bloom corresponds with a phase lag
to a nitrate minimum. The latter is followed by a phosphate maximum, which
is in good accordance with the fact that phosphate is the growth limiting factor
in that case. Hence the phytoplankton consume first the most available nutrient,



which is nitrate in our case. Indeed, other growth-limiting factors such as light,
temperature as well as grazing pressure from zooplankton are also important for
phytoplankton. All data are not yet completely analysed at this stage and in order
to understand the nutrient cycling through the eutrophic lake ecosystem, long term
field measurements are required (Karafistan et al. 1998). When all measurements
are synthesized, rates and fluxes of nutrients transported through each compartment
will be estimated. These data will then be used as input in a one-dimensional (1D) physico-chemical water quality model in order to predict the feature behaviour
relevant to this lacustrine ecosystem. Model will be 1-D, since the water is considered to be completely mixed and each station seems to have completely different
characteristics depending on the polluting sources. In sedimentation basins such as
Lake Manyas, retention of nutrients is also possible. Residence time of water and
renewal characteristics will be taken into account in the study of dispersion of
pollution. The final results will help in monitoring, conservation and restoration
measures to be taken.
Besides the conventional physical and bio-geochemical water quality properties, the microbiological ones were also our particular concern for Lake Manyas
as a natural reserve. We have demonstrated that the heterotrophic activity of some
nitrogen fixing indicator bacteria continue even in winter. This should be due to
favourable conditions such as the availability of nitrogenous products. It was also
noticed that the microbial regeneration of nitrogen occurs throughout the year,
reaching its highest level in winter. Sulphate was also found to be high in December. These properties will be incorporated to the water quality model mentioned
above. Even though pathogenic sewage organisms do not live long in water, purification is absolutely necessary. From our observations we have also revealed the
need for more measurements and data concerning the previous hydrological regime, geographical, meteorological and topographic parameters, as well as remote
sensing observations, surrounding land and water uses.
As a sound protection and a first management plan we have recommended to
the Scientific and Technological Research Council of Turkey (TUBITAK) that first
of all the water regime should be returned to its previous natural level. With TUBITAKs intervention we have lately established contact with authorities in that
area. Our first hand results will be presented to the directorate of the museum
of the natural Park and the council of the municipality. As a management and
restoration plan the most polluting point sources will be urged for cooperation
in a sustainable purification program. Help from the gendarmerie will be asked
for control and surveillance. Other public authorities will also be notified on the
consequences of pollution in the lake. All purification plants should be operational.
To our knowledge the lake will be loaned for 4 years to the fishing cooperative of
Lake Manyas. Inconveniences of over fishing will be explained to the fishermen of
that area. School children will be educated on water quality and bathing conditions.
According to the latest good news, as a measure against B pollution, a reservoir for



collecting boric and other discharges in that area has been constructed recently and
it will soon be operational.
The results obtained thus far were also presented at the International Zoology
Conference (October 2325, 2003 Istanbul) dedicated to the 100th anniversary of
C. Kosswig.

Field work and laboratory analysis were funded by the Scientific and Technological
Research Council of Turkey, (TUBITAK, with project grant YDABAG 101Y118).
This work has also been realized with technical and financial support from the
Research Foundation of the Canakkale Onsekiz Mart University. We are grateful to
Research assistants S. Sagir, F. Cakir and D. Odabasi, the Museum of National Park
at Kus Cenneti, together with the Fisheries Union of Bereketli Village in Manyas,
environment protection (gendarmerie) unit of the municipality of Bandirma for
their kind help and information provided about the field area.

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