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Revista Científica UDO Agrícola Volumen 9. Número 3. Año 2009. Páginas: 681-699

 

Periphyton succession in a waste water treatment pond

 

Sucesión del perifiton en un tratamiento de aguas residuals

 

Alex Chuks CHINDAH  ¹, Solomon Amabaraye BRAIDE¹, Jonathan AMAKIRI² and Oluwakemi Okoba KIOLAWSON AJIBULU¹

 

¹Institute of Pollution Studies, Rivers State University of Science and Technology, Nkpolu Oroworukwo P M B 5080, Port Harcourt, Rivers State , Nigeria and ²Plant Science and Biotechnology, University of Port Harcourt, Choba, Rivers State, Nigeria. E-mails: alexchindah@yahoo.com    Corresponding author

 

 

ABSTRACT

 

A study on periphyton succession in the self-depuration wastewater body exposed to sunlight was conducted for 15 days in a laboratory pond. The physico-chemical parameters (temperature, pH, salinity, conductivity, turbidity, total dissolved solids, total suspended solids, nitrate, phosphate and sulphate) and biological parameters (periphyton) were determined. The changes observed in some of the physico-chemical variables indicated a reduction in biochemical oxygen demand (BOD) (96%), chemical oxygen demand (COD) (96%), nitrate (93%), phosphate (81%) and sulphate 55%. Periphyton standing stock was 6.31 x 10⁶ indiv L^-1 at day 15. pH and dissolved oxygen (DO) showed strong linearity with periphyton standing stock and biomass. The standing stock and biomass had a positive relationship with the species dominance index, and an inverse relationship with species diversity. Linear regression model predicted 70% and 64% potential changes in the periphyton biomass that might be attributed to pH, DO and BOD, and NO₃^-, PO₄ ^-3, and SO₄^2-, respectively. The periphyton assemblages shifted in dominance from one algal form to another through out the exposure time, with a total of 50 algal species encountered during the study. The successional patterns of the periphyton community revealed that Oscillatoria terebriformis, Lyngbya pseudospirulina, Chlamydomonas reinhardtii, Euglena pascheri, Lepocinclis steinii and Oscillatoria chalybaea are useful as bioindicators of municipal wastewater.

 

Key words: Periphyton, Succession, waste water, treatment, sunlight

 

RESUMEN

 

Se condujo un estudio sobre la suceción del perifiton en la autodepuración de un cuerpo de aguas residuales expuesto a la luz solar durante 15 días en un estanque tipo laboratorio. Se determinaron parámteros físicos (temperatura, pH, salinidad, conductividad, turbidez, sólidos disueltos totales, sólidos suspendidos totales, nitrato, fosfato y sulfato) y parámetros biológicos. Los cambios observados en algunas de las variables físico-químicas indicaron una reducción en la demanda bioquímica de oxígeno (DBO) (96%), demanda química de oxígeno (DQO) (96%), nitrato (93%), fosfato (81%) y sulfato (55%). El máximo standing stock de 6.31 x 10⁶ indiv L^-1 se observó para el perifiton Algunos parámetros físico-químicos tales como pH y oxígeno disuelto (OD) mostraron una fuerte asociación lineal con el standing stock del perifiton y la biomasa. El standing stock y la biomasa tuvieron una relación directa positiva con el índice de la dominancia de especies pero exhibieron una relación inversa con la diversidad de especies. Los patrones sucecionales de la comunidad del perifiton revelaron que that Oscillatoria terebriformis, Lyngbya pseudospirulina,  Chlamydomonas reinhardtii, Euglena pascheri, Lepocinclis steinii y Oscillatoria chalybaea son útiles como bioindicadores de las aguas residuales municipales. El modelo de regresión lineal predijo los cambios potenciales en la biomasa del perifiton que puede ser atribuido al pH, DO y BOD en 70% y NO₃^-, PO₄ ^-3 y SO₄^2- en 64%. La composición del perifiton cambió en la dominancia de una forma algal a otra a través del tiempo de exposición con un total de 50 especies del perifiton encontradas durante el estudio.

 

Palabras clave: Perifiton, succesión, aguas residuales, tratamiento, luz solar.

 

INTRODUCTION

 

The increasing human population and activities such as expansion of urban centres and industrial setups have resulted in the generation of different waste types that are discharged into surface water bodies. Much of these are in solid and liquid forms consisting of domestic organic and inorganic wastes, spent oil (crank caseoil), and agricultural pesticides and fertilizers. The magnitude of these wastes has in recent times increased several folds and is now of concern to all the stakeholders including the scientific community (SC), non-governmental agencies (NGO), government agencies (GA) and other citizens (Chindah 1998).

 

One of the freshwater bodies impacted by these activities is the Nta-wogba stream that receives several point and non-point sources of untreated industrial and municipal wastes. The stream finally empties into the brackish water bodies where its impacts on water quality and biological resources resulting in loss of water integrity, aesthetics and biodiversity.

 

This freshwater ecosystem is apriori capable of self-purification through biological processes (Lakatos et al., 1997), which depends largely on the physiographic features of the stream and climatic conditions as wastes received and discharged are within the carrying capacity of the system (Soler et al., 1991). Under this circumstance, the effluent load is small and thus capable of elimination of organic and inorganic pollutants by decomposition and the absorption of inorganic compounds, through the simultaneous physicochemical and biological processes (EPA 1983, 1987). With the discharges from these municipal and industrial settings being overwhelming, results in the inability of the system to carry the extraneous organic and inorganic load with the concomitant loss of integrity and the goods and services which it provides.

 

In spite of increasing trend in the magnitude of wastes discharged into the natural environment and the threat posed to these resources as a result of human activities, little has been achieved in respect of waste treatment process and the physicochemical and biological interplay in Nigeria (Chindah et al., 2005; Chindah et al., 2007). Most of the previous studies mainly focused on the status of water qualities (RPI, 1985, IPS 1990, NDES, 2000, NDDC, 2004,) and level of contaminants on water resources (Ajayi and Osibanjo, 1981; Ndiokwere 1984; Ibiebele et al., 1987; Ekweozor et al., 1987; Powell 1987; Ekweozor et al., 1987; Amadi et al., 1997; Okpokwasili and Nwabuzor 1988; Okpokwasili and Olisa, 1991; Chindah, 1998; Joiris and Azokwu 1999; Chindah and Sibeudu, 2003).

 

Little is however known on wastewater self–depuration that practically requires no external energy other than sunlight, as well as, oxygen which is essential for the decomposition of organic matter and is provided in high proportion by the photosynthetic activities of the microbial communities present in the system (Abeliovich 1986).

 

Greater efficiency of the treatment is achieved when the microbes used in the treatment process are aerobic bioreactors (algae, protozoa or bacteria) and their optimum environmental conditions for growth provided (EPA 1990 and  2002).

 

Some of these studies have implicated periphyton as possible candidate in wastewater treatment and are gaining worldwide attention (Soler et al., 1991; Laktos et al., 1997; EPA 2002). In most developed world, the use of stabilization ponds as a biological system has assumed great importance based on its economy in wastewater management and usefulness in production of microorganisms that mineralize the organic and inorganic components (Oswald 1988 and Ogan 1988).

 

In order to bridge the existing gap at Nta-Wogba is located on the western flank of Port Harcourt city of the Rivers State, Nigeria this area, this study was undertaken to monitor water quality and successional patterns of periphyton assemblages with the view of identifying possible indicator species relating to changes in water quality during the treatment process.

 

MATERIALS AND METHODS

 

Study area

 

The Nta-Wogba is located on the western flank of Port Harcourt city of the Rivers State, Nigeria. The stream lies between latitude 40 50" and 50 00"N and longitude 60 55" and 70 00"E (Figure 1.). The climate of the area is that of tropical equatorial latitude with rainfall occurring almost all year round (Gobo 1998; Gobo et al., 2008). The Nta-wogba is a black water stream with its head water draining the Ora-Azi forest, and meanders through the densely populated city of Port Harcourt into the Bonny estuary.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

The stream system is exposed to increasing amount of urban wastes as it flows seaward, mainly from industrial and domestic discharges from laundry, photographic studios, garages, and wastes from markets and construction sites. The human activities exert considerable negative impact on the entire study area.  It is estimated that the water body receives about 4500 L/day of waste containing petroleum product, especially from crankcase oil, over 250,000 L/day from domestic waste, 80 kg/day of human waste, 20 kg/day of metal, and 58 kg/day of solid waste such as paper and polyethylene bags.

 

Rainfall occurs almost all the months (May - November) of the year with short duration of dry season (December -April) and an annual average rainfall of 2360mm (Gobo 1988 and Gobo et. al, 2008). The natural drainage basin is largely exposed as vegetation is virtually removed by adjacent development with the fringe and water surface covered by macrophytes such as Nymphaea micrantha, N. lotus,  Pistia stratiotes, Eclipta prostrate, Torulinium odoratum, Ludwigia leptocarpa, L. erecta, Ipomea aquatica, Neptuna oleracea , Saccioleis Africana, Cyperus distans, and C. sphacelatus (Chindah et al., 2005; Izonfuo et al., 2005)

 

Experimentation

 

Water from the study station was collected in pre-cleaned 50 litre plastic jerry cans to fill two triplicate 50 L polyethylene tanks in the laboratory. The tanks were left in an open and wide area to avoid shading at all times. From the tanks, samples for water quality and biological analysis were conducted for a period of two months. Slide panels in rack were placed in each of the tanks. The slides were examined under binocular microscope on each day for the assessment of periphyton.

 

Sampling collection and laboratory procedures

 

Physicochemical Parameters

 

Samples were collected daily with 2ml plastic containers at sub-surface level and analyzed in the Institute of Pollution Studies (IPS) laboratory using procedures as outlined in Standard methods for the examination of water and wastewater (10). Temperature was measured using a mercury bulb thermometer. pH was measured with a pH meter (Hanna instrument model HI8314). The conductivity was measured using the Horiba water checker model U-10. Dissolved oxygen (DO), and biochemical oxygen demand (BOD₅) and chemical oxygen demand (COD) were determined using Winkler’s method as described in APHA (1998). Other parameters such as ammonia-nitrogen (NH₃-N), nitrate-nitrogen (NO₃-N), sulphate (SO₄^-2), and phosphate (PO₄^-3) concentrations were determined spectrophotometrically (Spectronic Spectrophotometer 21D), following the procedures as described in APHA (1998).

 

Biological Parameters

 

Periphyton

 

Periphyton was collected daily for a period of 15 days. For each treatment a total of 3 scrapings were taken by removing a slide from the rack seeded in the wastewater. An area of 1cm² from each slide was carefully scraped with a sharp edged scalpel. The first  scrapings was emptied into a plastic vial containing 20 ml of Lugol’s solution for species identification and numeric analysis; and the second scrapings was put in a glass vial containing 5ml  of 90% acetone for chlorophyll a analysis (biomass).

 

From the original stock sample, duplicate samples for numerical analysis were obtained by collecting 1ml sub-sample of the properly homogenized sample with a Stampel pipette. The content transferred into a Sedgewick–Rafter counting chamber for enumeration at a microscope magnification of 400x, and identification at magnification of 1000x using the reports of Mills (1932) Sieminiska (1964) Starmach (1974) Patrick and Reimer (1966) Durand and Leveque (1980) and Chindah and Pudo (1991).

 

The chlorophyll a pigment (as mg chlorophyll cm^-2) was determined following Standard methods (APHA 1998). Upon removal from the slides the material was immediately transferred to labeled tubes containing  5ml of acetone, which was added to the sample in the plastic vials. This was centrifuged at 450rpm . The supernatant was carefully transferred to a glass cuvette and absorption measured at 630nm, 645nm and 660nm using spectrophotometer (Spectronic 21D).

 

 

Statistical analysis

 

Species richness, species diversity index, dominance and evenness were analyzed as indicated below.

 

The species diversity index was determined using the Shannon-weaver's (1964) function H′ given by the equation:

 

H′ = - Σ (ni/N) Log (ni/N) i

        

Where:

 

ni = The number of species in group (i),

N = Total number of species in (i) group.

 

The specie dominance index was calculated using the Bergen-parker dominance index (Chellappa 1990):

 

d = n_max/N_T

 

 

Where:   

 

n_{max =} number of individuals of the dominant species,

N_{T  =}   total number of individuals of all the species recorded.

 

Physico-chemical and biological parameters were analyzed using 2-way analysis of variance (ANOVA). F-test, was conducted evaluate any significant difference between days.  Inter-relationship between physicochemical and biological attributes was evaluated using Excel package 2003. Regression model was used to predict the relationships between the actual and expected values amongst some critical variables (physicochemical and biological parameters)   and all calculations were performed for n = 16 observations.

 

RESULTS

 

Physicochemical parameters

 

The synopsis of physico-chemical changes observed during the treatment process is presented in Table 1.

 

 

 

 

 

Table 1. Physicochemical variables in the wastewater treatment system from Diobu in Port Harcourt, Nigeria.
S/no parameter	Range	Mean and SD	% Recovery
Temperature (ºC)	26.5 - 32	29.24 ± 2.16	ND
pH	7.2 - 9.0	7.91 ± 0.50	80.00*
Conductivity (µScm-1)	506 - 706	620.87 ± 70.26	72.94
Turbidity (NTU)	3 - 62	22.67 ± 13.36	95.2
TDS ( mg L-1)	358 - 494	440.2 ± 45.81	27.1
TSS ( mg L-1)	1.74 - 3.19	2.746 ± 0.52	45.5
DO ( mg L-1)	0.23 - 6.00	2.01  ± 2.15	96,0
BOD5 ( mg L-1)	0.92 - 28.5	16.25  ±11.86	96.8
COD ( mg L-1)	0.81 - 19.95	11.38 ± 8.31	96.8
Nitrate ( mg L-1)	0.04 - 0.64	0.22  ±  0.16	93.75
Phosphate ( mg L-1)	0.39 - 4.54	2.83   ± 1.36	91.4
Sulphate ( mg L-1)	8.81 - 16.01	12.46 ±2.82	45.9
ND – not determined, * increased value

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Biological parameters

 

Species occurrence and successional patterns

 

A total of 50 taxonomic species occurred in the periphyton. These species were represented by Chlorophyceae (17 species), Cyanophyceae (14 species), Bacillariophyceae (11 species) and Euglenophyceae (8 species) (Table 2 and Figure 2). Generally, the emergence of species in the periphyton community differed from one species to another species (Figure 2).

 

 

 

Table 2. The periphyton species observed in the treatment tank during the depuration study
Family	Species
Cyanophyceae	Anabaena flos-aquae (Lyng) Breb Anabaenopsis arnoldis Aptkarj Anacystis aeuroginosa Kütz. Chroococcus turgidus (Kützing) Nägeli Rhabdoderma lineare Schmidle et Lauterborn Oscillatoria chalybaea (Mertens) Gom. Oscillatoria terebriformis (Ag.) Gom.	Chroococus minuta Skuja Gloeocapsa magna (Breb) Kütz Gomphosperia aponina Kütz. Lyngbya pseudospirulina Pascher Merismopedia punctata  Meyen Oscillatoria okenii (Ag.) Gom. Romeria elegans (Wolosz.) Kocz
Chlorophyceae	Chlamydomonas reinhardtii  P.A. Dangeard Chloromonas ulla (Skuja) Gerloff et Ettl. Euastropsis richteri (Schmidle) Lagerheim. Scenedesmus acornis (Ehr.) Scenedesmus quadricauda  (Turpin) Breb. Scenedesmus ovalternus (Bernard) Chodat Scenedesmus obliquus (Breb) Playfair Scenedesmus pseudoarmatus T. Hortobágyi Roya cambrica West & G.S.West	Ulothrix limnetica Lemmerman Closterium incurvum Bréb. Closterium limneticum  Lemm. Cosmarium pyramidatum Bréb Coelastrella levicostata Korshikov Phacotus lendneri Chodat Tetradesmus crocici  Fott et Kom Staurastrum apiculatus (Scott & Prescott) Croasdale & Scott
Euglenphyceae	Phacus granum Drezepolski Phacus acuminatus Stokes Phacus pleuronectes (O.F. Müller) Duj. Trachelomonas zuberi Koczwara	Euglena acus Ehr. Euglena pascheri Swirenko Lepocinclis teres (Schmitz)  Francé Lepocinclis steinii Lemm.
Bacillariophyceae	Achnanthes linearis (W. Sm.) Grun. Achnanthes exigua Grun. Pinnularia maior (Kützing) Cleve Synedra ulna (Nitzsch) Ehr. Synedra acus Kütz Nitzschia linearis (C.A. Agardh) W. Smith.	Synedra parasitica (W. Smith) Hustedt Navicula minima Grun. Navicula mutica Kütz. Navicula cuspida Kutz. Navicula lanceolate (Ag.) Kütz.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

The species dominant in the early stage of the study (1-2days) were euglenin forms (Euglena pascheri, E. acus, and Phacus acuminatus) and constituted 77.5% of the periphyton community. Thereafter, the euglenin population quickly declined. The decline observed, euglenin was promptly occupied notably by green algal forms (Chlamydomonas spp. and Chlormonas ulla) in day 3 and 4, they constituted about 54.5% of the population. The presence of these forms gradually faded and was replaced by the cyanobacteria, which represented 62% to 87.9% of the periphyton standing stock. Amongst the cyanobacteria, the dominant species were Anacystis aeuroginosa, Oscillatoria terebriformis, O. chlalybaea, and Lyngbya pseudospirulina (Figure 2). The gradual disappearance of the blue green algae gave rise to diatoms on day 14. The dominant diatom species were Synedra acus, S. parasitica, Navicula minima, N. mutica, Nitzschia linearis, Achnanthes linearis, and they constituted 83% of the periphyton standing stock (Figure 2).

 

Species richness fluctuated considerably, maintained almost uniform value for the first 2 days (14 species) before an increase to the day 4 (21 species) subsequently declined on the day 5 (15 species) before another increase and stable value between 6^th and the 7th day (22 species). After the 7th day a depression in species number was observed on the 8th day (10 species) and species richness increased steadily to attain the second peak on the 10th day (23 species), declined slightly before attaining the maximum value of 50 species to the end of the experiment (Figure 3a).The species diversity increased initially to the 4^th day and fluctuated there after demonstrated similar pattern as described for species richness but the peaks (minimum and maximum) did not occur on the same days (Figure 3b). While species dominance index was stable from day1 to day 9 (0.0022), the value increased sharply on day 10 (0.2825) and fluctuated thereafter to the end of the study (Figure 3b) such that dominance index and species richness demonstrated inverse relationship with the other (Figure 3b).

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Changes were observed in the periphyton community structure pattern that demonstrated variability at different stages with first development being the encrusting of Euglenophyceae (72.8-77.6%), followed by the entrant of Chlorophyceae from day 3 to 4 (44.8-54.5%). Cyanophyceae dominated the periphyton community from day 5 to 11(62-87%), while Bacillariophyceae was observed from day 12 to 15 (57.6-83%), in that respective order (Figure 4). These episodic dominance by major taxonomic groups influenced  series of patterns observed, such that at the early (day 1 to 2) stages,   encrustation pattern was in the decreasing order of Euglenophyceae (77.6%) > Cyanophyceae (14.2%) > Chlorophyceae (8.2%) Bacillariophyceae (0%).  Thereafter the changes in encrustation progressed at the mid stages particularly on the 8^th day with a community structure pattern of Cyanophyceae (54.4%) > chlorophyceae (22.6%) > Euglenophyceae (19.5%) > Bacillariophyceae (3.5%). At the end of the study another shift in community structure was observed which followed a sequence of Bacillariophyceae (57.6%) > chlorophyceae (39.4%) > Cyanophyceae (1.7%) > Euglenophyceae (1.2%) respectively (Figure 4).

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Periphyton standing stock was observed to maintain the same trend as was observed for species dominance index pattern throughout the study duration. The highest standing crop of (63111 × 10² indiv/cm²) was obtained on day 10, while the least standing crop of (287 × 10² indiv/cm²) was obtained on day 8 of the study (Figure 5a). It was observed that, periphyton standing stock had direct relationship with dominance index (D), but exhibited inverse relationship with species diversity index (H').

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Periphyton Biomass (chlorophyll a)

 

Similarly, chlorophyll a increased from a minimum of (0.0033mg/cm²) on day 2 to a remarkable maximum increase (1.6994 mg/cm²) on day. The chlorophyll a concentration also demonstrated a strong affinity with species dominance index and standing stock (Fig. 5b).

 

Amongst the periphyton descriptors chlorophyll a (R²= 0.66) was the best regressed followed by periphyton densities (R²= 0.47), Species richness (R²= 0.24), species diversity (R²= 0.16) = species dominance index (R²= 0.16)

 

 The correlation coefficient recorded some relationship between the dependent and independent (physicochemical and biological attribute). Strong positive relationships were observed between exposure period and biomass (chlorophyll a), DO, pH, abundance, and dominance index. Chlorophyll a exhibited strong positively correlation with DO, pH, abundance and Dominance index. Other strong positive relationships were that between PO₄ with Conductivity and TDS, SO4 with conductivity, turbidity, and TDS and pH with Dominance index. Moderate positive associations were observed between conductivity with turbidity and TDS; BOD₅ with conductivity, turbidity, TDS, and TSS; NO₃ with conductivity, turbidity, and TSS, SO4 with NO₃ and PO₄; pH with DO and abundance; and PO₄ with Species diversity. Low positive relationships were observed between Turbidity and TDS; NO₃ with BOD₅, COD, and PO₄; DO with temperature, abundance and dominance index; and SO₄ with COD. Strong inverse relationship were also observed such as the relationship between exposure period with conductivity, TDS, NO₃, PO₄,and SO₄; chlorophyll "a" with conductivity, TDS,PO₄; pH with Conductivity, TDS, NO₃ and SO₄; Species diversity with abundance and dominance index. Moderate inverse relationships were observed between exposure period with Turbidity, BOD₅, and COD; chlorophyll a with turbidity, BOD, NO₃, SO₄ and COD; Conductivity with DO, abundance, and dominance index; DO with conductivity, turbidity, DO, COD and TDS; TDS with DO, abundance and dominance index; TSS with COD; PO4 with pH, abundance, and dominance index; SO₄ with abundance, dominance index; pH with COD and species diversity index. Low negative associations were observed only between species diversity with exposure period and chlorophyll a.

 

The linear regression model

 

The predictions on the response of different water quality parameters during the exposure time and the relationships with the actual data set from this study were analyzed using the linear regression model presented in Figures 6a-j.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

The model showed the relationship between chlorophyll a and some measured attributes indicated that while some attributes such as exposure time, DO, dominance index, PO₄, pH, and SO₄ were more strongly correlated to the changes in chlorophyll a as they explained 90, 77, 76, 74 72 and 67% of the variation respectively (as expressed in equations 1, 2, 3, 4, 5 and 6).

 

Equation 1:

 

Chlorophyll a = 0.1177(t) - 0.3079 (r2= 0.90)

 

Where t is duration of exposure, r² (90%) being changes in chlorophyll a attributed to exposure period.

 

Equation 2:

 

Chlorophyll a = 0.2081DO + 0.2153 (r=0.77)

 

Equation 3:

 

Chlorophyll a = 4.9688SDI + 0.3019 (r = 0.76)

 

Equation 4:

 

Chlorophyll a = -0.316PO4 + 1.5298 (r =0.74)

 

Equation 5:

 

Chlorophyll a = 0.8422_(pH) - 6.0308, (r = 0.72)

 

Equation 6:

 

Chlorophyll a = -0.1399SO4 + 2.3769 (r = 0.67)

 

While other contributors with relatively weaker contribution to changes in chlorophyll a are  NO3, COD, BOD, species diversity with contributing influence to in the order of 58, 54 , 53 and 48% respectively (as expressed in equations 7, 8, 9 and 10).

 

Equation 7:

 

Chlorophyll a = -2.0475(NO3) + 1.1034 (r = 0.58)

 

Equation 8:

 

Chlorophyll a = -0.038 (COD) + 1.0658 (0.54)

 

Equation 9:

 

Chlorophyll a = -0.0266(BOD) + 1.066 (r = 0.53)

 

Equation 10:

 

Chlorophyll a = = -11.095(SDI) + 1.6215 (r = 0.48)

 

In addition, chlorophyll a  as biomass can be predicted from a combination of some  critical water quality attributes (DO, BOD and pH) as represented by a linear regression model in Equation 11): 

 

Equation 11:

 

Chlorophyll a = - 3880 + 0.1553_Do + 0.0054_BOD + 0.5207_pH,  r² = 0.7007, n = 15. 

 

This indicated significantly that 70% of the changes in the chlorophyll a concentration could be attributed to the values of DO, BOD, and pH in the wastewater.

 

Similarly, the prediction can also be defined, using nutrient parameters (N0_3, P0_4, and S0₄) and is represented by a linear regression model in Equation 12.

 

Equation 12:

 

Chlorophyll – a =1.9636 – 0.8620_N03 - 0.0215_P04 - 0.0419_S04, r²= 0.6485

 

Thus, 64% of the changes in the Chlorophyll  a can be attributed to P0_4, S0_4, and N0₃ values on the coefficient of determination r².

 

          

 

DISCUSSION

 

The physico-chemical changes observed during the treatment process demonstrated considerable changes for most of the parameters as reported earlier in a separate report (Chindah et. al. 2005)

 

The total number of species encountered in the periphyton community during the study was lower than that observed for the phytoplankton in the same treatment medium (Chindah et al., 2007). The reasons for the differences may be associated with the fact that all the emerging species in medium may not be periphytic in nature. However, most of the species observed in the periphyton community have been reported in natural stream systems in the Niger Delta region (Chindah 1998; Chindah et al., 1999b). The lower number of species richness observed in the treatment medium vis-à-vis that of natural water bodies is expected due to continuous and longer period of exposure and interaction with changes in the water regimes. Nonetheless the phytoplankton pooled higher species richness than the periphyton community that recorded lower species richness. This differences observed in species richness may be associated with the duration as there may not have been adequate retention as is the case in natural water bodies (Chindah 2003: Chindah et al., 1999b).  

 

         The observed increase over time in periphyton species recruitment and development of periphyton community suggest that such increment in species probably may be alluded to individual species requirement to changes in nutrients and other important environmental gradient factors regulating the pattern observed in the tank. These factors probably are responsible for the observed sequence in the entrant of these species at certain water quality.  This is possibly evidence supporting the response and preference of periphyton species to different water quality. Such predilection influence recruitment pattern as previously reported for phytoplankton community under similar circumstance (Chindah, 2007), but the periphyton community differed in some of the species types and in the recruitment and prosperity pattern. This observation corroborates findings of other scholars that reported distinct changes in periphyton community as the nutrient gradient progresses (Lakos et al., 1997; Pringle 1990; Pan et al., 2000; Hillebrand and Sommer, 2000).

 

The initial occurrence of euglenins, green and blue green algal species especially the species of Oscillatoria terebriformis, Lyngbya pseudospirulina,  Chlamydomonas reinhardtii. Euglena pascheri, Lepocinclis steinii, and Oscillatoria chalybaea suggest that these are not sensitive species and or species that are resistant and or indifferent to such increases or even favored by such conditions (opportunistic species) as the municipal wastewater stressors. Those species therefore are more tolerant to the stressor where excluded from the population and can be classified as tolerant species.  This also qualifies these species as indicator species for waste water monitoring.

 

However, the later emergence of diatom species that were absent in the early stages suggest that the waste water contains contaminants that negatively suppress the development of these species that were absent at the early stages. This observation is congruent with remarks on other studies in crude oil contaminated environment (Amadi et al., 1997; Chindah 1998; Pudo and Fubara 1998; Chindah et al., 1999b).  EPA (2002) contends that municipal and industrial wastes favour the occurrence and preponderance of some algal species over others especially those species that have the ability to tolerate unfavorable and extreme conditions. However the composition of species at the end of the study is similar to trends observed in natural soft acid freshwater system (Chindah 2003). Thus the improved complexity in species composition in the periphyton community provided ample evidence suggesting that the depuration resulted in improved water quality thus responsible for improved status in periphyton species richness and its diversity. This is in consonance with the observation of Eloranta, 1999 who observed that diatoms community reacts with changes in water quality within a few days.

 

Species richness and diversity were observed to decrease and increase in an oscillating pattern but in relatively similar manner throughout the study. This pattern observed may be associated with the shifts in dominance of the periphyton community. This is in agreement with previous findings in a freshwater stream by Stevenson et al., (1991), Hillebrand and Sommer (2000ab), Stevenson et al., (1991) and who independently observed that decreases in diversity with colonization time was due to an increased dominance of some algal species. However, Falomo (1988), Hilleband et al., (2000) and McCormick (2001) attributed such changes in marine environment to alterations in nutrient levels. The high species dominance index is indicative of the high nutrient concentration and periphyton standing stock in the wastewater. This result and those by Boyton et al., 1983; Falomo 1988; Stevenson et al., 1991 and Sabater et al., 1998) confirm that proliferation of algal species resulted in  high dominance index. Consequently an inverse relationship was observed between species dominance index and species richness and species diversity index,

 

The shift observed in the community structure from the beginning to the end of the study such that Cyanophyceae >Bacillariophyceae > Euglenophyceae > Chlorophyceae in decreasing order of importance is similar to other studies on the impact of sewage discharges on the water quality and periphyton communities (Pudo 1985; Chindah 1998 and Chindah et al., 1999b). The observed reversal in role in the community structure from the early to the middle and to the end of the study suggests on one hand that changes of individual species of different taxonomic groups and abundance over time and on the other hand on competitive ability for nutrient, substrate surface area and light availability. Earlier studies (Jackson 1977; Hoagland et al., 1982 and Chindah et al., 1999b) reported similar results in their periphyton assemblages.

 

The dominance of the diatoms species at the later stages of the experiment is indicative of its positive response to increase DO and reduced BOD₅ and nutrient levels, which connotes improved water quality status. Conversely, the early dominance of euglenin and blue green algae species is indicative of its firstly attributed to there preference or tolerance of low pH and DO and high BOD₅ and nutrient suggesting poor water quality. This result is in agreement with previous reports by Amadi et al., (1997), Chindah (1998) and EPA (1990, 2002), that the preponderance of blue algae over other forms is indicative of an altered community structure and poor water quality and   the   increase of   diatoms species is suggestive of a community that had attained stability (Chindah et al., 2007).  

 

            The periphyton standing stock and biomass were exceptionally higher on day 8 and 10 than those from other days. This may be attributable to the preponderance of blue green algal forms over others during the corresponding period.  There have been similar findings by other researchers on primary producers, positing that high proportions of blue green algae contributed significantly to periphyton abundance and biomass (Brock 1985; Pudo et al., 1988; Pudo 1989; Vymazal and Richardson 1995). 

 

However, Soler et al., (1991) in their studies observed that high biomass concentration coincided with the blooms of chlamydomonas (green algae) in self-depuration of wastewater body. Form our study; it is difficult to draw such conclusions as maximum chlorophyll a was observed when there were reasonable entrants of species from other family groups in the periphyton community.  It is therefore possible to suggest that chlorophyll a concentration in wastewater treatment system dependent on the blooms of the different species possibly due to the fact that the present study did not consider other chlorophyll types.

 

The periphyton standing stock and biomass were higher than those reported in natural black water stream in the region, with considerable lower nutrient quality status (Chindah 2003; Amadi et al., 1997). It is therefore possible, to associate the differences in periphyton standing stock and biomass to nutrients. This observation is in agreement with earlier reports by Borchardt (1996) that reported that high nutrient availability in a medium yielded high periphyton abundance and biomass.

 

The inter-relationships of the physiochemical and biological parameters as reflected in the correlation coefficient matrix that gives an overview of the role of the water quality variables on the periphyton community. The strong positive associated observed between exposure period and some biological attributes (Biomass, chlorophyll a), abundance, and dominance index and physicochemical variable (DO, pH,) suggested that exposure time played a key role on these attributes.  Other similar strong positive association such as the relationship between biomass (chlorophyll a) in one hand with DO and pH; and secondly with   abundance and dominance index implies that these attributes are important and fundamental characteristics in monitoring periphyton in waste water treatment. The medium and low positive associations explained elsewhere in this study demonstrate the critical role played by each of the variable and this is expected in natural phenomenon. Conversely, the strong negative relationship between the concentrations of some nutrient parameters such as PO₄ and SO4 with species diversity, dominance index and periphyton abundance leads to the conclusion, that periphyton species diversity, dominance index   and abundance, are favourable under nutrient limitation (Peterson and Grimm, 1992; Alcoverro et al., 2000). This phenomenon is attributed to relevance of the nutrient imbalance in the production of extracellular polymeric substances by the benthic or resuspended diatoms under nutrient limitation as posited by Alcoverro et al., 2000. Generally it is pertinent to suggest that while some of the variables constitute a defining factor critical to the depuration process, others appear to be of less environmental consequences to the system. This result agrees with previous studies that periphyton biomass decline with increase in nutrient availability and increase in grazing pressure by epizooic species (McCormick and O¢Dell 1996; Pan et al., 2000; EPA, 2002).

 

The critical associations observed between the periphyton and water quality highlight the importance of water quality and environmental gradient on the organization of biological resources and the close relationship between the predicted and actual data implies that these parameters can be relied upon in waste water treatment monitoring as they provide understanding of the possible ecologic effects of anthropogenic activities and ecosystem stability.  It is the belief of the authors that the study has provided a framework in which ecological processes can be manipulated to achieve a desired phytoplankton community that identifies successional activities and dynamic factors influencing succession in a restoring singularly applied treatments.

 

It is therefore possible to suggest that while some of the variables are critical to the depuration process, others appear to be of less environmental consequences to the system. The predictive model allowed us to conclude that calculations based on biomass are good descriptors of the studied system, although other units could be preferentially used in other environments.

 

 

CONCLUSION

 

The changes observed in some of the physiochemical and biological parameters in this study are suggestive of the recovery of a wastewater body and such as the reduction of biological oxygen demand, Chemical oxygen demand, Nitrate and Phosphate concentrations, as well as the increase in species composition of periphyton assemblages that are indicative of a more stable aquatic environment.

 

The periphyton standing stock and biomass have direct relationship with species dominance, but exhibit inverse relationship with species diversity.

 

The detection of the pattern of succession of euglenins → green algae → blue green algae → diatoms, is a very useful tool to discern the stages of the depuration and detect possible future changes in the composition of the periphyton community.

 

ACKNOWLEDGEMENT

We are grateful to the staff of the Institute of Pollution Studies (IPS), Rivers State University of Science and Technology, Port Harcourt chiefly U. J. Ikoro, Hanson Uyi, Nathan Nario and Uchenna Anireh for their support and assistance during the laboratory studies. The collaborations of J. N. Onwuteaka, A. Osuamkpe and I. Cookey especially during the compilation and analysis are greatly acknowledged.

 

LITERATURE CITED

 

Abeliovich A. 1986. Algae in wastewater oxidation ponds: In Handbook of microalgal mass culture. Richmond .A (ed.) pp331-338. CRC press, Boca Raton, Fla, USA.

 

Ajayi S. O. and A. Osibanjo. 1981. Pollution studies on Nigerian Rivers 11. Water quality of some Nigerian Rivers.  Environ.  Pollut 1981, (Series B) 2: 87-95.

 

Alcoverro, T.; E. Conte and L. Mazzella. 2000. Production of mucilage by the Adriatic epipelic diatom Cylindrotheca closterium (Bacillariophyceae) under nutrient limitation. Journal of Phycology 36: 1087-1095.

 

Amadi E. N.; A. C. Chindah and C. C. Ugoji. 1997.  The effect of municipal profainage on the microflora of a black water stream in Port Harcourt, Nigeria. Niger Delta Biologia 2 (1): 125-139.

 

American Public Health Association (APHA). 1998. Standard methods for the evaluation of water and waste water. 2th ed, Washington: American Public Health Association.

 

Brock T. D. 1985. Phytoplankton. In: T. D. Brock (ed): A Eutrophic lake, Lake Mendota, Wisconsin. New York, Springer -Verl. p. 85-114.

 

Borchardt M. A. 1996. Nutrients In: R. J. Stevenson, M. L. Bothwell and R. L. Lowe (Eds): Algal ecology (Freshwater Benthic Ecosystems). San Diego: Academic Press. p. 184-228.

 

Chellapa N. T. 1990.  Phytoplankton species composition, chlorophyll biomass, and primary production of the jundai reservoir (north eastern Brazil) before and after entrophication. J. Acta  Hydrobiol. 32 (1/2): 75-91.

 

Chindah A. C. 1998. The effect of Industrial activities on the periphyton community at the upper reaches of New Calabar River, Niger Delta, Nigeria. Wat. Res. 32 (4): 1137-1143.

 

Chindah, A. C. 2003. The physico-chemistry phytoplankton and periphyton of a swamp forest streams in the lower Niger Delta. Scientia Africana 2 (1&2): 106-116.

 

Chindah A. C. and J. Pudo. 1991. A preliminary checklist of algae found in plankton in Niger Delta, Nigeria.  Frag. Flor. Geobot. 36 (1): 112-126.

 

Chindah, A.C. and O. C. Sibeudu. 2003. Levels of hydrocarbons and heavy metals in sediment and a decapod crustacean (Crab – Uca Tangeri  ). In: The Bonny/New Calabar River Estuary, Niger Delta. Pol. Journal of Environmental Protection 25/26, 55-71.

 

Chindah, A. C.; A. I. Hart and B. Atuzie. 1999a.  A preliminary Investigation on effects of municipal waste discharge on the Macro fauna associated with macrophytes in a small fresh water stream in Nigeria. African Journal of Applied Zoology 2: 29-33.

 

Chindah A. C.; A. I. Hart and A. Uzoma. 1999b. Periphyton associated with submerged macrophyte Crinium natans) in the upper reaches of the new Calabar River, Niger Delta. Agric Biotech  Environ, 1 (2):  37-46.

 

Chindah, A. C.; S. A. Braide and E. Izundu. 2005. Treatment of municipal wastewater quality using sunlight. Caderno de Pesquisa. Ser. Bio. (Santa Cruz do Sul) 17 (2): 27-45.

 

Chindah, A. C.; S. A. Braide, J. Amakiri and E. Izundu, E. 2007. Succession of phytoplankton in a municipal waste water treatment system under sunlight. Revista Cientifica UDO Agricola 7 (1): 258-273.

 

Durand J. R. and C. Levegue. 1980.  Flora et fauna aquatiques de 1’ Afrique.  Cah off  Rech.  Scio Tech.  Outre Mer, 1 : 5-46.

 

Ekweozor, I. K. E.; A. Ugbome and E. I. Ombu. 1987. The effects of chronic oil pollution in the central Bonny esturary. Proceedings of 1987 seminar on the Petroleum Industry and the Nigerian Environmnet, Nov. 9-12. PortHarcourt. p. 198-207.

 

EPA 1983. Municipal wastewater stabilization ponds: Design manual. United States Environmental protection Agency, Municipal environmental Laboratory.  Cincinnati, Ohio. EPA/625/1-83-015.

 

EPA 1987. Report on the use of Wetlands for Municipal wastewater treatment and disposal. United States Environmental protection Agency Washington, DC. EPA/430/09-88-005.

 

EPA 1990. Impacts on quality of inland wetlands of the United States: A survey of Indicators Techniques and Applications of community level Biomonitoring Data. United States Environmental protection Agency Washington, DC. EPA/600/3-90/073

 

EPA  2002. Methods for evaluating wetlands condition: Using Algae to Assess Environmental conditions in wetlands. Office of Water. United States Environmental protection Agency Washington, DC. EPA-822-R-02-021

 

Eloranta P, 1999. Applications of diatoms indices in Finish rivers. In J.Prygiel, B.A.Whitton and Bukoswska J. (eds), Use of algae in monitoring rivers III. – Agence de l’Eau Artois-Picardic, Douai p. 138-144.

 

Falomo, R. O. 1998.  The impact of industrial effluents in the distribution of plankton of the Central Bonny Estuary.  M. Sc.  Thesis, Rivers State University of Science and Technology.

 

Gobo, A. E. 1988. Relationship between rainfall trends and flooding in the Niger-Benue river Basins. J. Metrology 13: 13.

 

Gobo, A. E.; I. U. Ubong and P. N. Ede. 2008. Rainfall intensity analysis as a tool for hydrological and Agricultural practices in Southern Nigeria. The International Journal of Meterology 33 (334): 344-350.

 

Hillebramd H. and U. Sommer. 2000a. Effects of continuous nutrient enrichment on microalgae colonizing hard substrates.  Hydrobiologia 426: 185-192.

 

Hillebrand H. and Sommer U. 2000b. Diversity of benthic Microalgae in response to colonization time and eutrophication. Aquatic Bet. 67: 221-236.

 

Hillbrand H.; B. Worm and H. K. Lotze. 2000.  Marine microbenthic community structure regulated by nitrogen loading and grazing pressure Mar. Ecol.  Prog.  Ser. 204:  27-28.

 

Hoagland, K. D.; S. C. Roemer and J. R. Rosowski. 1982.  Colonization and community structure of two periphyton assemblages, with emphasis on the diatoms (Bacillariophyceae).  Am. J. Bot 69: 188-213.

 

Ibiebele D. D.; S. A. Braide, A. C. Chindah and F. O. Harry. 1987. Oshika oil spill incident: Case study four years after the spill. In Proceedings of the 1987 Seminar on the Petroleum Industry and the Nigerian. Environment. p. 126-132.

 

Institute of Pollution Studies (IPS). 1990. Ecological post impact studies of Ebubu-Ochani oil spillage. Institute of Pollution studies Rivers State University of Science and Technology, PortHarcourt Rivers State of Nigeria. RSUST/IPS/TR/90/02, 232 pp.

 

Izonfuo, W. A. L.; A. C. Chindah, S. A. Braide and D. Lawson. A. 2005.  Physicochemical characteristics of different ecotonal streams in a rapidly developing metropolis in the Niger Delta, Nigeria. Caderno de Pesquisa. Ser. Bio. (Santa Cruz do Sul Vol) 17 (2): 91-105.

 

Jackson J. B. C. 1977. Competition on marine hard substrates: The adaptive significance of solitary and colonial strategies. Amer. Nat. 111: 743-797.

 

Joiris, C, and M. I. Azokwu. 1999. Heavy metals in the bivalve Anadara (Senilia senilis) from Nigeria. Mar. Pollut. Bull. 38 (7): 618-622.

 

Lakatos G.; M. K. Kiss, M. Kiss and P. Juha´sz. 1997. Application of constructed wetlands for wastewater treatment in Hungary. Wat. Res. 15 (5): 341-346.

 

McCormick P. V. and M. B. O’Dell. 1996. Quantifying periphyton responses of phosphorus in the florida Everglades: A synoptic- experimental approach. J .N Am. Benthol. Soc 15: 450-468.

 

McCormick P. V.; M. B. O’Dell, P. B. E. Shuford, J. G. Backus and G. Kennedy. 2001. Periphyton responses to experimental phosphorus enrichment in subtropical Wetland. Aquatic Bot. Vol. 71 (2): 119-139.

 

Mills, F. W. 1932.  Some diatoms from Warri, South Nigeria. Jour. Roy. Microse, 582: 383-395.

 

Ndiokwere, C. L. 1984. An investigation of heavy metal content of sediments and algae from the River Niger and Atlantic coastal water. Environ.Pollut. (B) 7: 247-254.

 

Niger Delta Environmental Survey (NDES). 2000. Ecological zonation and habitat  classification. 2^nd Phase  Report 2, Vol.1: 1-66.

 

Niger Delta Development Commission (NDDC). 2004. Biodiversity of the Niger Delta Environment Niger Delta Development commission master plan Project Final report.

 

Ogan, M. T. 1988. Examination of surface water used as source of supply in PortHarcourt area: II. Chemical hydrology. Arch. Hydrobiol. 79 (2/3): 25-342.

 

Okpokwasili, G. C. and A. C. Olisa. 1991. Riverwater biogradation of surfactants in detergents and shampoos. Water Res. 25 (11): 1425-1429.

 

Okpokwasili, G. C and C. N. Nwabuzor. 1988. Primary biodegradation of anionic surfactants in laundary detergents. Chemosphere 17: 2175-2182.

 

Oswald W. J. 1988.  Micro-algae and wastewater treatment.  In Micro-Algae Biotechnology.  M. A. Borowitzka and L. J. Borowitzka (Eds), p. 305-328.  Cambridge University press.

 

Pan Y.; R. J. Stevenson, P. Vaithiyanathan, J. Slate and C. J. Richardson. 2000. Changes in algal assemblages along observed and experimental phosphorus gradients in a subtropical wetland, Freshw. Biol. 43: 1-15.

 

Patrick R. and C. Reimar. 1966.  The diatoms of the United States excluding Alaska, and Hawaii, fragilariaceae, Eunotiaceae, Achnanthaceae, Naviculaceae.  688 pp.  The Living Stone Publication, Philadelphia, USA.

 

Peterson. C. G. and N. B. Grimm. 1992. Temporal variation in enrichment effects during periphyton successsion in a nitrogen-limited desert stream ecosystem. J. N. Am. Benthol Soc. 11 (1):  20-36.

 

Pringle C. M. 1990. Nutrient spatial heterogenity effects on community structure, physiognomy, and diversity of stream algae. Ecology 71: 905-920.

 

Powell, C. B. 1987. Effects of freshwater oil spillages on fish and fisheries. The Proceedings of 1987 Seminar on the Petroleum Industry and the Nigerian Environment.

 

Pudo J. 1985. Investigation on algae in the oil spilled region of the Bonny River. In: Proc. Ecolog. Society of Nigeria Annual Conference. Nigeria: Port Harcourt. p. 171-177.

 

Pudo J. K. and D. M. J. Fubara. 1988. Studies in the periphyton algae in the petroleum spillage area of the Niger aquatic system.  Veih.  Inter. Ver. Limnol 23; 2259-2261.

 

Pudo J. 1989. Ekologiczne skiki zanicezyszcznia ropa naflowa poludniowej Nigerii (South Nigeria -ecological consequence of crude oil water pollution) Gosp Wodna 4: 85-87.

 

Reseasch Planning Institute (RPI) 1985. Columbia South Carolina, USA. Environmnetal Baseline Studies for the establishment of Control Criteria and Standars against Petroleum Related Industries in Nigeria. RPI/R/84/4/15-17.

 

Sabater, S.; J. S. V. Gregory and J. R. Sedell. 1998.  Community dynamics and metabolism of benthic algae colonizing wood and rock substrata in a forest stream.  J. Phycol 34: 561-567.

 

Shannon C. E and W. Weaver. 1964. The mathematical theory of communication. Illinois, Urbana press, 125pp.

 

Sieminiska’s, 1964.  Chrycophyta 11 Bacillariophyceae.  Okrzemia In:  K. star Mach (ed) Flora Slokowodna Polski: Fresh waterflora of Poland”  4.502 pp.

 

Soler, A.; J. Saez, M. Llorens, I. Martinez, F. Torrella and L. Berna. 1991. Changes in physico-chemical parameters and photosynthetic microorganisms in a deep wastewater self-depuration lagoon. Wat. Res., 25 (6): 689-695.

 

Starmach, K. 1975.  Chytophyceae – Kryptofity, Dinophyceae-dirofity, Raphidophyceae – rafidofoty – In: “flora of poland” 4. 502 pp. Parnstwowe, whydawnietwo, Nankowe, Warszawa (in polish).

 

Stevenson, R. J.; C. G. Peterson, D. B. Kirschtel, C. C. King and N. C. Tuchman. 1991.  Density dependent growth, ecological strategies and effects of nutrients and shading on benthic diatoms succession in streams.  J. Phycol. 27: 59-69.

 

Vyzamal J. and C. J. Richardson. 1995. Species composition, biomass and nutrient content of periphyton in the Florida Everglades. J. Phycol. 31: 343-354.

 

 

 

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