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Tropical Freshwater Biology, 23 (2014) 21 - 37

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http://www.ajol.info/index.php/tfb; DOI: http://dx.doi.org/10.4314/tfb.v23i1.2
INFLUENCE OF CLARIAS GARIEPINUS (TEUGELS) CAGE CULTURES
ON WATER QUALITY, PHYTOPLANKTON AND PERIPHYTON
COMPOSITION: A CASE STUDY OF AHMADU BELLO UNIVERSITY
RESERVOIR, NIGERIA
S. J. Oniye a, Y. Tanimu a, A.M. Chia a,b* and D. Yusuf a
a

Department of Biological Sciences


Ahmadu Bello University, Zaria, Nigeria.
Postal code: 810001
b

Laboratrio de Cianobactrias, Escola Superior de Agricultura Luiz de Queiroz,


University of So Paulo, Piracicaba-SP, Brazil. CEP: 13418-900
* Corresponding author: chia28us@yahoo.com/machia@usp.br
ABSTRACT

Water quality, periphyton and phytoplankton growing as a function Clarias


gariepinus (Burchell, 1822) cage cultures have rarely been investigated. Physical
and chemical factors associated with cage culture of Clarias gariepinus in
relation to phytoplankton and periphyton were examined fortnightly from May to
June 2009 in the Ahmadu Bello University reservoir. Phytoplankton abundance
based on divisions showed that Chlorophyta > Bacillariophyta > Cyanophyta,
while for periphyton Chlorophyta > Euglenophyta > Cyanophyta >
Bacillariophyta. Community structure analyses showed that species diversity was
highest in the cages, while species dominance was highest on the bamboo raft
periphyton community. Phytoplankton and periphyton distribution and abundance
was closely related to the physicochemical characteristics of the water especially
nitrate and phosphate concentrations. The physicochemical parameters were
within acceptable limits for fisheries, and algal composition posed no risk to the
cultivated fish and the reservoir.
Keywords: physicochemical parameters, microalgae, cyanobacteria, aquaculture,
artificial substrates

Trop. Freshwat. Biol. 0795-0101/14/15USD 2014 Idodo Umeh Publishers Ltd., Nigeria

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S. J. Oniye et al.
INTRODUCTION

Among the various culture systems, integrated aquaculture is considered as a


sustainable small scale aquaculture system. The nature of integration may be of
various types, the integrated cage fish culture technique is relatively new and
innovative (Mondal et al., 2010). Fish can be reared in cages that usually apply to use
of already existing water bodies that cannot be drained or seined, what would
otherwise not be suited for aquaculture (Onyema, 2011; Ayroza et al., 2013). Cage
aquaculture has certain advantages over other aquaculture systems that are potentially
important in terms of uptake by rural poor and landless people; use of existing ponds,
lakes and reservoirs that are currently not utilized; ease of feeding; ease of stocking
and harvesting; less expense associated with treating or preventing disease; easier
stock management and monitoring compared with pond culture (Mondal et al., 2010;
Onyema, 2011). However, fish-farm nutrient enrichment from incomplete
consumption of food by farmed fish and the excretion of nitrogenous compounds
affect the environment by modifying the physical and chemical characteristics in the
surrounding area (Sara, 2007; Mannino and Sara, 2008). These result in changes in the
water column and sediment chemistry (Kalantzi and Karakassis, 2006). As a result,
periphyton and phytoplankton communities associated with this environment elicit
responses that can be tied to these variations in their immediate environment (Chia et
al., 2011a, 2012; Bere et al., 2012).
Colonization referred to as periphyton or algal fouling by local infra-upperlittoral benthic communities can provide reliable records of water chemistry
effects (Angel and Spanier, 2002). The worldwide availability of artificial hard
surfaces like buoys and cage structures provide substrata for the recruitment of many
intertidal benthic organisms (Mannino and Sara, 2008). Only a few studies have dealt
with the phytoplankton and periphyton communities associated with cage cultures of
Clarias gariepinus in tropical inland freshwater reservoirs. In addition, there is
paucity of information about the fish farming waste impact of water chemistry on
periphyton growing on artificial substrata with which cages are made and its role as a
bioindicator. Thus, the phytoplantonic and periphytonic communities, due to their
ability to integrate biotic and abiotic factors over time, are capable of responding
directly to changes in environmental variables, resulting in sensitive bioindicators of
ecosystem changes at smaller spatial scales (Mannino and Sara, 2008; Bere and
Tundisi, 2011).
Despite the investigation by Amisah et al. (2008) on the importance of
periphytonic based fish production, nothing was given on the periphytonic and
phytoplanktonic community composition associated with the Clarias gariepinus cage
culture system. Onyema (2011) contributed to the knowledge of periphyton
community structure of cage cultures associated with Lagos lagoon in South Western
Nigeria. However, the water chemistry of Lagos lagoon is significantly different from
that of Ahmadu Bello University (ABU) reservoir in terms of salinity and other
chemical parameters, considering the various sources that contribute to its water

Fish cage culture effect on microalgal community

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volume. Due to the paucity of information, the periphyton-based system can already
be seen among pond fish farmers that they are still subject to investigations for
improvement to obtain sustainable and diversified benefits. In conservation practices
of fish, poor fishers might benefit if they get more information on substrate,
periphyton and phytoplankton that are closely related to this system. Most studies on
cage cultures rarely report on the phytoplankton and periphyton communities. Hence,
investigations were conducted to determine the phytoplankton and periphyton
communities associated with Clarias gariepinus cage cultures in the Ahmadu Bello
University (ABU) reservoir, Zaria, Nigeria.
STUDY AREA
The study was carried out in the Ahmadu Bello University (ABU) reservoir, Zaria
(Longitude 7o 38 N and Latitude 11o 11E, Fig. 1). The reservoir was constructed in
1974 to provide portable water for the university community; it has a maximum
capacity of 1.603 million litres. The reservoir has an approximate width of 122 m and
a mean depth of 6 m. The activities around the ABU reservoir are regulated by the
University Authority. Mahogany trees are planted within the immediate catchment
area of the reservoir and its tributaries, as a watershed management strategy. Farming
and other anthropogenic activities around the reservoir (and upstream) are prohibited
to protect the reservoir from siltation and excessive addition of agro-allied chemicals.
Fishing is restricted to registered fishermen and; the reservoir has been an important
research laboratory for fisheries and limnology students over the years.
MATERIALS AND METHODS
Cage culture system design and experimental setup
The construction of the cage followed the design of Otubusin (1985). The cage culture
comprised a 3 set of six (6) cages made of bamboo, each supported with two (2)
plastic floats by the sides. Each set of six cages was held in place by a bamboo raft
and had 1 m3 volume. The three sets were arranged in a parallel manner. The cages
were rectangular in shape and made of bamboo lattices walls with lockable lids. The
mesh size (12.7 mm mesh size) was small enough to prevent the experimental fish
from escaping, although this permitted water to easily pass through the cages.
Physicochemical parameters
Physiochemical parameters were analyzed fortnightly for six weeks at two weeks
intervals from May to June 2009. This period represented the last months of the cage
culture experiment and also the last growth phase of the Clarias gariepinus. This
experiment was prompted by the visible appearance of microalgal growth around the
cage culture, and the need to explain the possible relationship between the

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S. J. Oniye et al.

Fig.1: Map of Zaria-Nigeria showing the location of Ahmadu Bello University


Reservoir (Dam).
physicochemical characteristics and microalgal growth, and what implication this may
have on fish health. Water temperature (WT) was measured in situ using a mercury
thermometer. pH and electrical conductivity (EC) were measured using Hanna
instrument (model 210). Water hardness (WH) was determined using EDTA
titrimetric method as described by APHA (1998). Dissolved oxygen (DO) and
biological oxygen demand (BOD) were determined by the Azide modification of the
Winkler method (Lind, 1979). Nitrate-nitrogen (NO3-N) was determined by the
Phenoldisulphonic acid method (Mackreth, 1963), phosphate-phosphorus (PO4-P) was
analyzed by using the Ammonium Molybdate method (APHA, 1998)

Fish cage culture effect on microalgal community

25

Algal collection
Phytoplankton were collected using a conical shaped plankton net of 20 cm diameters
and 60 mL collection vial, at three sampling points in a triangle around the cages.
Periphyton were collected by gently scraping three replicates of 1 cm2 surfaces of the
bamboo cages, bamboo raft and plastic floats of the cages. Algal samples were
preserved in Lugols iodine solution. Algae were identified using relevant online
identification resources and keys such as Presscott (1977) and APHA (1998) as
identification guides. Algal cell densities were calculated using the drop count
technique (Chia et al., 2011a).
Statistical analyses
Data for physicochemical and biological parameters were subjected to Analysis of
Variance (ANOVA) to test for significant differences in their means over time and
within sampling stations. Significantly different means were separated using Duncan
Multiple Range Test (DMRT) Post Hoc test. Canonical correspondence analysis
(CCA) using inter-species distances and biplot scaling was used to establish
significant correlations between the physicochemical characteristics and
phytoplankton and periphyton data. Using 1000 unrestricted permutations, the Monte
Carlo permutation test was used to test for the significance of the CCA. Species
dominance, Simpson, Shannon diversity indices, Evenness, Margalef and Fisher alpha
were used to determine the phytoplankton and periphyton community structure.
ANOVA and DMRT were done using Statistica version 8.0 for windows. CCA and
Monte Carlo permutation tests were done using Canoco 4.5 statistical package and
community structure analysis was done using PAST v.2.09 for window.
RESULTS
Water temperature was 300.33oC, water hardness 1.74 0.36 mg L-1 and electrical
conductivity 70.360.80 S cm-1 (Table 1). Dissolved oxygen and BOD
concentrations were lower during the last two samplings, and both had mean values of
7.060.16mg L-1 and 2.120.49 mg L-1, respectively. Nutrient (NO 3-N and PO4-P)
concentrations were higher as the study progressed than at the start of the experiment,
while pH remained within the neutral range having a mean value of 7.060.23. Of all
physicochemical parameters measured in this study, the concentration of NO3-N and
pH values varied significantly over time. Water temperature and water hardness
varied significantly temporally and spatially. All the physicochemical parameters
analyzed varied significantly either over time or space except for dissolved oxygen
that showed no significant difference under all the conditions tested (Table 1; p >
0.05). Phytoplankton and periphyton taxonomic group variations are shown in Fig. 2.
The chlorophyta division predominated in both phytoplankton (ca. 80%) and
periphyton (ca. 66%) communities; and was followed by the bacillariophyta (ca. 17%)

26

S. J. Oniye et al.

Fig. 2: Relative abundance of different phytoplankton and periphyton groups recorded


in the water and associated with the cages throughout the study.
Spirotaenia sp. that were found only on the plastic float and the bamboo raft. The
chlorophyta was the most diverse group having eleven different individuals, while the
bacillariophyta, cyanophyta and euglenophyta were represented by three, two and two
representatives, respectively (Table 2). Community structure analyses showed that of
all communities of algae and cyanobacteria analyzed, species dominance was highest
on the raft substrate and closely followed by the float substrate (Table 3). Fisher
alpha, Simpson and Shannon diversity indices were highest in the cage substrate or
surfaces and closely followed by the phytoplankton species community. Margalef
index was highest in the cage and raft material. Species evenness was generally higher
in the cage periphyton and phytoplankton communities (Table 3).
Figures 3 to 6 show the correlation matrix based PCA for the relationship of
different periphyton and phytoplankton species with the physicochemical
characteristics of water. Characteristics like NO3-N, pH, EC, PO4-P and WH showed
significant association with the following phytoplankton species Spirogyra sp.,
Oedogonium sp., Hydrodictyon sp. and Tribonema sp. in the first component and
Oscillatoria sp., Stigoclorium sp. and Synedra sp. in the second CCA component. A
significant positive relationship was recorded between Diatoma sp. and Closterium sp.
with water temperature, BOD and DO (Fig. 3). Desmodium sp., Diatoma sp.,
Spirogyra sp. and Mougeotia sp. had a significant positive relationship with water

Mean physicochemical characteristics of Ahmadu Bello University reservoir during the study period
Week

1
3
5
MeanSD
ANOVA Time
(p value)
ANOVA Station
(p value)

Water
Temperature
(0C)

Water
Hardness
(mg L-1)

Electrical
Conductivity
(S cm-1)

Dissolved
Oxygen
(mg L-1)

Biochemical
Oxygen
Demand
(mg L-1)

NO3-N
(mg L-1)

PO4-P
(mg L-1)

pH

30.67

1.03

69.17

7.37

3.1

0.24

0.24

6.59

29.67

2.07

71.88

6.82

1.48

0.31

0.28

7.35

29.67

2.13

70.03

1.78

0.31

0.26

7.25

300.33

1.740.36

70.360.80

7.060.16

2.120.49

0.290.02

0.260.01

7.060.23

0.00

0.01

0.11

0.76

0.09

0.01

0.35

0.00

0.00

0.02

0.05

0.27

0.19

0.06

0.03

0.28

Fish cage culture effect on microalgal community

TABLE 1

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S. J. Oniye et al.

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TABLE 2
Periphyton and Phytoplankton species distribution in the different substrates recorded
in this study.
Classification
Bacillariophyta
Diatoma sp.
Synedra sp.
Achnantes sp.
Tribonema sp.
Chlorophyta
Oedogonium sp.
Spirogyra sp.
Hydrodictyon sp.
Desmidium sp.
Closterium sp.
Stigeoclonium sp.
Genicularia sp.
Mougeotia sp.
Spirotaenia sp.
Ulothrix sp.
Chroococcus sp.
Cyanophyta
Oscillatoria sp.
Merismopedia sp.
Euglenophyta
Euglena sp.
Lepocinclis sp.

Abbreviation

Plastic float

Bamboo raft

Bamboo cage

Phytoplankton

Dia
Syn
Ach
Trib

+
+
+
+

+
+

+
+
-

Oed
Spi
Hyd
Des
Clo
Sti
Gen
Mou
Spt
Ulo
Chr

+
+
+
+
+

+
+
+
+
+
+
+
+
-

+
+
-

+
+
+
+
+
+
+
-

Osc
Mer

+
+

+
-

+
-

Eug
Lep

+
-

+
+

+ means species is present and means species is absent


hardness, nitrate nitrogen, electrical conductivity and pH; and a negative relationship
with BOD, water temperature, and DO (Fig. 4). The periphyton community associated
with the floats showed that only Ulothrix sp. had a significant positive relationship
with DO, BOD and water temperature (Fig. 5). The relationship between cage
periphyton and physicochemical parameters (Fig. 6) showed that Spirotaenia sp.
Bumilleriopsis sp. Chaetophora sp, Characium sp. Agmenella and Desmodium sp.
were significantly positively associated with DO, water temperature and BOD.
Spirogyra sp., Ulothrix sp., Tribonema sp., Draparnaldia sp. Chroococcus sp. and
Euglena sp. were significantly positively associated with pH, nitrate nitrogen, water
hardness and phosphorus. In all the CCAs, at least 60% of the total variation was
accounted for by the first two CCA components.

Fish cage culture effect on microalgal community

29

TABLE 3
Microalgal and cyanobacterial community indices in the different substrates
investigated.
Diversity indices
Phytoplankton
Periphyton
ANOVA
P- value
Raft
Float
Cage
Taxa_S
12
14
13
18
Dominance_D
0.13
0.24
0.20
0.15
0.01
Simpson_1-D
0.87
0.76
0.80
0.85
0.01
Shannon_H
2.24
1.81
1.84
2.22
0.01
Evenness_e^H/S
0.78
0.43
0.48
0.51
0.01
Margalef
2.26
2.49
2.17
3.13
0.04
Equitability_J
0.90
0.68
0.72
0.77
0.01
Fisher_alpha
3.23
3.51
2.90
4.58
0.04

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S. J. Oniye et al

Fig. 3: CCA biplot showing the association of different physicochemical parameters


with phytoplankton species associated with cage cultures in Zaria, Nigeria.

Fish cage culture effect on microalgal community

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Fig. 4: CCA biplot showing the correlation of different periphyton species on the cage
culture raft with physicochemical characteristics of the water in Ahmadu Bello
University reservoir, Zaria, Nigeria.

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S. J. Oniye et al

Fig. 5: The relationship between periphyton species on the cage culture floats
and physicochemical parameters of Ahmadu Bello University reservoir water,
Zaria, Nigeria shown using CCA biplot.

Fish cage culture effect on microalgal community

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Fig. 6: CCA biplot showing the association of different periphyton species on


the cages with the physicochemistry of Ahmadu Bello University reservoir
during the study period.
DISCUSSION
Increasing nutrient load observed over the study period may be connected with
anthropogenic additions of artificial feed for the Clarias gariepinus. Hall et al. (1992)
and Kaggwa et al. (2011) reported that only 31% of of N and P that is added through
feed are removed at harvest, the rest being released as fish faesces, urinary waste and
uneaten feed. Similar to Kaggwa et al. (2011), despite the nutrient variation over time,
no significant differences were observed between the cages for nitrate concentration.
However, phosphates had a different trend by varying significantly between the
different stations. These similarities between the different cages may be due to
flushing that may have occurred when it rains bringing about dilution and dispersal of
accumulated waste. It is common to observe wild fish feeding on unconsumed feed by

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S. J. Oniye et al.

the cultured fish. This may have reduced any accumulation and excessive increase in
nutrients that is associated with the cage culture system in the reservoir as it already
contains other fish species. Although, the concentrations of these nutrients were
within adequate levels capable of stimulating phytoplankton growth (Reynolds, 2006;
Tiseer et al., 2008; Chia et al., 2011a, 2012).
The mean surface water temperature varied slightly during the study period
and fell within the 25 to 36 oC optimal growth temperature range for fish culture,
which is similar to what is obtainable at Zaria Dam which is about 25 Km from ABU
reservoir (Oniye et al., 2002) and most lenthic water bodies in Zaria (Chia et al.,
2009a,b, 2011a,b, 2012). Temperature affects the solubility of oxygen and
physiological processes of algae, zooplankton and fish. The significant positive
correlation between cage periphyton species abundance and water temperature may be
attributed to the fact that temperature is the driving force for many metabolic
processes and an increase in temperature may lead to increased metabolic activities
and consequently abundance of algae. Fish and other aquatic organisms require
dissolved oxygen for respiratory and other metabolic processes. DO concentration in
water is also dependent on atmospheric contact, photosynthesis by algae and other
aquatic plant, and activities of aerobic bacteria. The DO of ABU reservoir was found
to be within the allowable limits for fisheries and aquatic life in the EU (5.0 9.5),
Russia and elsewhere (4.0 6.0) (UNESCO, WHO and UNEP, 1996; Bunlipatanon et
al., 2014). The low BOD5 (1.48 to 3.10) of the ABU reservoir is indicative of low
pollution, as BOD5 represents the amount of oxygen utilized by aerobic bacteria in
decomposition of organic wastes. The pH of the reservoir falls within the range of 6.0
to 8.5 that is optimal for production of fish in the tropics (WHO/UNESCO/UNEP,
1996; Oniye et al., 2002). pH affects several other water parameters like metal
solubility and speciation that have very important structural and metabolic functions,
for example the metal Mg in the chlorophyll molecule and Cu as an enzyme co-factor.
The total hardness of the reservoir was lower than the desirable levels for fish culture
20 mg/L to 300 mg/L (Yisa, 2006).
The advantages conferred by adding feed to a cage culture system is an
increase in the energy, nutrient transfer efficiencies and growth of fish; additionally,
the effects of the periphyton and phytoplankton are alternate naturally available diet
for the fish, thereby reducing the cost of feed and hence, increasing economic returns.
In this study the bamboo cages, raffs and plastic floats formed a good substrates on
which the periphyton and phytoplankton flourished. Azim et al. (2001) and Amisah et
al. (2008) reported that natural solid substrates like bamboo and other tree branches
constitute an essential part of the periphyton-based aquaculture because of their
bacterial and zooplanktonic biomass inductive ability linked to microalgae and
cyanobacteria growth. This abundant natural food is exploited directly by many
herbivorous, carnivorous and omnivorous aquatic organism, particularly fish as a
basic source of food.

Fish cage culture effect on microalgal community

35

The high species diversity indices values, abundance of phytoplankton and


periphyton, and low species dominance are an indication of high productivity of the
ABU reservoir or at least the cages and their immediate surroundings, thereby giving
credence to the ability of this water body to support semi intensive fish farming,
particularly cage culture of Clarias gariepinus (Huda et al., 2002; Davies et al.,
2009). Algae are primary producers in the aquatic environments and thus at the base
of the food chain providing food for zooplankton, fish and other aquatic organisms. In
addition, the predominance of chlorophyta over other groups like the cyanobacterial is
a positive sign as the former is known to be more palatable to zooplankton and
herbivorous fish compared to the later. Huda et al. (2002) reported that introducing
logs of wood to stimulate algal growth was found to significantly increase economic
gain in fish culture. Algal species diversity and abundance is affected by the
physicochemical characteristics of the water in which they grow, as such they are
important bioindicators of water quality (Shehata et al., 2009). This explains the
significant association found between most phytoplankton and periphyton species
with physicochemical characteristics in this study. Venkateswarlu and Reddy (2000)
associated high abundance of the chlorophyta with clean waters, this places the
water in the reservoir of the ABU reservoir as a relatively clean water. Similar
results were obtained by Rodrigues and Bicudo (2009) who found that the major
floristic composition of periphytic algae was mainly influenced by environment type
(whether lotic or lentic) and water regime but not by type of growth surface. Hence,
several interacting factors may be responsible for the preponderance of periphyton and
phytoplankton in ABU reservoir and not substrate types only.
In conclusion, the physicochemical and biological parameters analyzed in this
study show that the use of Clarias gariepinus cage cultures in ABU reservoir
represents a possible viable source of semi-intensive fish cultivation. The
predominance of chlorophyta over other phytoplankton and periphyton groups means
that the reservoir water can sustain the growth of herbivorous and omnivorous fish
species without immediate risk of pollution if production level is sustained as semiintensive.
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