2679 Journal of Applied Sciences Research, 8(5): 2679-2688, 2012 ISSN 1819-544X This is a refereed journal and all articles are professionally screened and reviewed

ORIGINAL ARTICLES

Investigation on Mutual Relations between Bacteria and Zooplankton in Branch, River ,

Nehad Khalifa and Shawky Z. Sabae

National Institute of Oceanography and Fisheries, 101 Kasr Al Ainy, P.C. 11694, , (Egypt)

ABSTRACT

The importance of bacterioplankton and how it interplays with the classical food chain as food for zooplankton has gained considerable attention. This study aimed to investigate the relationship between bacteria and zooplankton in relation to some environmental variables at Damietta Branch of River Nile from spring 2008 to winter 2009. Microbiological examinations included total viable bacterial counts (TVBCs) at 22C and 37C, the bacterial biomass, in addition to the bacterial indicators of pollution, total coliforms (TC), faecal coliforms (FC) and faecal streptococci (FS). Bacterial biomass ranged from 0.29 to 8.42 mg C m–3 and bacterial indicators exceeded the acceptable level at some sites. In addition, the zooplankton populations recorded were clearly dominated by Rotifera (80.8%) and Protozoa (13.5), while crustacean zooplankton including cladocerans and copepods formed only 5.3 % of the total population. In general, the results indicated that there is a predominantly opposite relationship between bacteria and main zooplankton groups (Rotifera and Protozoa) in spring.

Key words: River Nile; Damietta Branch; Bacteria; zooplankton.

Introduction

River Nile is the main water supply for drinking purposes, irrigation and industry in Egypt. The ecology of River Nile ecosystem has been changed as a result of several factors including the construction of the High Dam, industrial development and pollution by domestic, industrial and agricultural wastes. Damietta Branch is extended from Delta Barrage to Mediterranean Sea; it is considered the second longest part of the Nile River (Moussa and Aziz, 2007). Damietta branch is about 242 km length, with an average width of 200 and an average depth of 12 metre. It is the main source of drinking and irrigation waters for El-Qalubia, El-Gharbyia, El-Dakahlyia and Damietta Governorates (Abdo, 2004). Damietta branch receives increasing amounts of waste discharges from several sources of pollution, industry, domestic and agriculture (APRP, 2002). Bacteria have been recently categorized as aquatic plankton after recognizing that they play an important role in secondary production via bacterial primary production. The concept of the microbial loop is that bacterial production can be comparable to primary production, and that the bacteria are consumed by micro and macrozooplankton. Several authors (Sanders et al., 1989; Vaque and Pace, 1992; Ooms-Wilms et al., 1995) concluded that bacterial standing crop can be suppressed by zooplankton grazing, i.e. that the microbial loop can experience top-down control, as occurs in the grazing food chain. Bacteria constitute an important food resource especially for protozoan, rotifer, and crustacean (Sherr and Sherr 2001, Yoshida et al., 2001). The growth rate of bacteria is known to be one of the fastest among unicellular organisms, if suitable conditions prevail. Despite such characteristics, however, in natural ecosystems, the bacterial abundance does not vary drastically but remain stable within a limited magnitude in a given ecosystem (Gurung et al. 2002). The higher grazing rate by microbial grazers implies the substantial role of material flux by bacterial production. Both laboratory and field studies have shown that grazing as well as resource supplies are important factors determining bacterial dynamics in aquatic ecosystems (Burns and Galbraith 2007). Zooplankton organisms are identified as important components of aquatic ecosystems. They help in regulating algal and microbial productivity through grazing and in the transfer of primary productivity to fish and other consumers (Dejen et al., 2004). Enteric bacteria, on the other hand, will experience high organic matter and nutrient concentrations and large changes in pH and oxygen availability during gut passage. The organic-rich, low oxygen environment inside a zooplankter’s gut and fecal pellets may favor anaerobic bacterial processes that are otherwise not feasible in the oxygenated water column. Indeed, an important observation in the past decades has been the presence of strict anaerobes inside the zooplankton gut and fecal pellets (Braun et al., 1999). Globally it is estimated that 12% of the primary production is consumed, directly or indirectly, by

Corresponding Author: Nehad Khalifa, National Institute of Oceanography and Fisheries, 101 Kasr Al Ainy, P.C. 11694, Cairo, (Egypt) E-mail: [email protected]; Fax: (+2) 02 42185320 Tel: (+2) 01008018481 2680 J. Appl. Sci. Res., 8(5): 2679-2688, 2012 metazoan zooplankton (Calbet, 2001). The zooplankton body provides protection to the associated bacteria from environmental stresses similar to biofilms. Furthermore, migration by zooplankton enables rapid dispersal of bacteria over vast distances and across boundaries such as the pycnocline. In addition to live zooplankton, molts, fecal pellets, and carcasses of zooplankton all influence water column and benthic microbial communities in various ways (Tang et al., 2009). Many studies have been conducted on the microbial quality and zooplankton abundance and its community structure of River Nile water or its branches, while no studies have been reported on the zooplankton bacterivory. Therefore, this paper aims to investigate the mutual relationship between the bacteria and zooplankton in relation to some environmental variables in Damietta Branch of River Nile.

Materials and Methods

Water samples for bacteriological analysis and zooplankton examination were collected from five sampling sites along Damietta Branch, River Nile in four successive seasons (spring 2008 - winter 2009). The sampling sites are Station 1 (Benha); Station 2 (); Station 3 (); Station 4 (El-Serw) and Station 5 (Faraskour) as shown in figure (1). Physicochemical parameters including, temperature, pH, electrical conductivity (EC), total dissolved solids (TDS) and dissolved oxygen (DO) were estimated by using the standard methods of APHA (1998).

Fig. 1: Map showing sampling sites at Damietta Branch of River Nile, Egypt.

Water samples, for bacteriological analyses, were collected in 500ml sterilized glass bottles from each sampling site (except at station 4 in spring season due to break of the sample) and transferred in an ice-box to the laboratory to be analysed. Bacteriological analyses included determination of the total viable bacterial counts (TVBCs) at incubation temperatures, 22C and 37C, using spread–plate method (APHA, 1998). The bacterial cell measurements were estimated using scanning electron microscope (Jeol, Jem-1200 EXII, Japan) and the cell volumes were then calculated according to the formula in Löffer-Kröβbacher et al. (1998). Then, the bacterioplankton biomass in mgCm-3 was calculated. The density of the total coliforms (TC), faecal coliforms (FC) and faecal streptococci (FS) were estimated MPN method. For determination of TC, water sample of 10 ml was inoculated in each of triplicate tubes containing 10 ml of double strength MacConkey broth and 1 and 0.1 ml of water sample were inoculated in triplicate tubes containing 5ml of single strength MacConkey broth. The inoculated tubes were incubated at 37oC for 48 hr. Positive tubes were indicated by the produced acid and gas. For FC three loops from positive tubes were subcultured in freshly prepared 5ml single MacConkey broth and then incubated in water-bath at 44oC. Positive tubes were confirmed by sub-culturing on Eosin-Methylene Blue (EMB) medium where coliform bacteria gave defined colonies with metallic sheen character. Most probable number (MPN) of faecal streptococci was determined using azide dextrose broth at 37oC for 48 hr. Positive

2681 J. Appl. Sci. Res., 8(5): 2679-2688, 2012 tubes were indicated by dense turbidity and confirmed by the formation of purple button at the bottom of the tube after incubation in ethyl violet azide dextrose broth at 37oC (Kamel, 1984). Zooplankton samples were collected from the selected sites by filtering 30 liters from surface water through a zooplankton net of 55 μm mesh diameter. Collected samples were kept in plastic bottles with some lake water to which 4% formalin was added as a preservative. Samples were studied under the compound microscope and specimens were identified at the species level when possible. Zooplankton numbers were expressed as number of organisms per cubic metres. The main taxonomic references used for identification of zooplankton were Edmondson (1963), Koste (1978) and Foissner and Berger (1996). Correlation coefficient was performed using Microsoft Excel to measure the relation between physicochemical parameters, bacterial indicators and zooplankton groups in order to verify the correlation between different variables.

Results and Discussion

The physicochemical properties of the collected water samples are shown in Table (1). The maximum water temperature was recorded during summer (32.4C), while the lowest (17.5C) was detected in winter. The decrease or increase in water temperature depends mainly on the climatic conditions, sampling times, sunshine hours and is also affected by specific characteristics of water environment such as turbidity, wind force, plant cover and humidity (Mahmoud, 2002). Hydrogen ion concentration (pH) is the master control parameter in aquatic environment for the chemical and biological transformation of water. It controls the solubility of metal ions and affects natural aquatic life. pH values of Damietta Branch water were in the alkaline side (7.25- 8.49). The relative decrease of pH values in winter season may be attributed to the lower activity of phytoplankton (Sabae, 2004). Seasonal variations in electric conductivity (EC) values ranged between 268 and 662 µmohs cm ̶ 1. The highest mean value (540 µmohs cm-1) was recorded during winter and the lowest mean value (308 µmohs cm ̶ 1) was recorded in spring. The maximum values of EC were recorded at stations 4 and 5 which may be attributed to the effluents discharged from El-Serw City and behind Faraskour dam Abdo (2004). The total dissolved solids (TDS) value fluctuated between 110 and 276 mg l ̶ 1 in the studied area (Table 1). The seasonal average showed that, there is an observed increase of TDS values in winter season, which may be due to lowering water level in River Nile during drought period which leads to concentration of dissolved minerals (Elsayed, 2009). Station 4 attained the highest TDS, which may be attributed to the effect of domestic and sewage effluents at El-Serw City (APRP, 2002). Dissolved oxygen (DO) is considered as an important parameter in assessment the degree of pollution in natural water. Dissolved oxygen values ranged between 4 and 8.86 mg l ̶ 1 during the study period. The lowest dissolved oxygen was recorded in summer, which may be attributed to high temperature of water which consequently increases the bacterial activity that degraded the organic matter at the expense of oxygen (Sabae and Ali, 2004). Station 4 attained the lowest dissolved oxygen and this may be due to wastewater discharged in this area which leads to increase of bacterial load which consumed the organic matter and uses available dissolved oxygen in this process, which agreed with the study of Abdo et al. (2010) on River Nile water.

Table 1: Range of physicochemical parameters of Damietta Branch during the studied period. Range Spring Summer Autumn Winter (Average) 2008 2008 2008 2009 Temperature (C) 24.5-25.5 31-32.4 18.4-20.5 17.5-18.9 (24.9) (31.8) (19.5) (18.2) pH 8.03-8.23 8.04-8.49 7.8-8.12 7.25-8.11 (8.12) (8.21) (7.98) (7.77) EC (µmohs cm-1) 272-347 268-377 434-529 460-662 (308) (326) (479) (540) TDS (mg l-1) 135-174 131-189 110-264 133-276 (154) (162) (192) (207) DO (mg l-1) 6.02-8.86 4-7.88 5.8-7.6 7-8.4 (7.01) (6.26) (6.52) (7.84)

Bacterial abundance varied from 3.1× 106 to 130 × 106 CFU ml–1 and from 3.8× 106 to 150 × 106 CFU ml–1 at 22C and 37C, respectively (Fig. 2 ). Meanwhile, bacterial biomass ranged from 0.29 to 12.16 mg C m– 3. Generally, the total bacterial counts increases from up-to downstream from Zefta to Faraskour, which may be attributed to domestic, sewage and agricultural effluents discharge into Damietta Branch (Fig. 3).

2682 J. Appl. Sci. Res., 8(5): 2679-2688, 2012

Fig. 2: Total viable bacterial counts (TVBCs) 10 6 CFU ml-1 at the selected sampling sites of Damietta Branch.

Fig. 3: Total bacterial biomass (mg C m-3) at the selected sampling sites of Damietta Branch.

The most probable number (MPN) of the total coliforms (TC), faecal coliforms (FC) and faecal streptococci (FS) are shown in table (2). It ranged between 29 - 8 000 and 24 - 930/100ml water for TC and FC, respectively. On the other hand, the most probable number of FS varied from 14 to 2900 /100ml water. European Commission Guide Standard (1998) and Ministry of Health, Egypt (1996) accepted the guide values of the investigated bacteria up to 500/100 ml water for TC and 100/100ml water for FC and FS. Thus, the indicator bacteria exceeded the acceptable level at some sites, which revealed that Damietta Branch waters subjected to sewage pollution. Seasonal variations showed that the high counts of bacterial indicators (TC, FC and FS) were detected in the warmer seasons (spring and summer), which may be attributed to increase of water temperature and discharge of waste water during these seasons (Sabae and Rabeh, 2007). A moderate positive relationship revealed between temperature and TC (r =0.555), while a weak ones were found with FC and FS. Dissolved oxygen is the best parameter for showing the effect of pollution on a river unless it contains toxic constituents (Laster, 1975). Regarding to the relation between oxygen concentration and different bacterial indicators,

2683 J. Appl. Sci. Res., 8(5): 2679-2688, 2012 moderate negative correlation found between oxygen concentration and TC (r=0.537). Ali et al. (2000) showed that FS had a negative correlation with oxygen concentration (r = - 0. 699) in River Nile. Total dissolved solid attained moderate positive relationship with bacterial count and bacterial biomass (r = 0.570 and 0.585), while no relationships was found between TSD and the faecal bacterial indicators.

Table 2: The most probable number (MPN) of total coliform (TC), faecal coliforms (FC) and faecal streptococci (FS)/ 100ml water of Damietta Branch. Stations Spring Summer Autumn Winter

TC FC FS TC FC FS TC FC FS TC FC FS

Benha 29 24 14 240 50 30 93 25 24 90 40 110 Zefta 36 24 210 250 80 40 45 40 110 45 40 110 Talkha 2400 550 280 8000 930 930 240 240 460 240 200 240 El-Serw - - - 1800 130 110 43 15 110 70 70 23 Faraskour 2400 930 2900 1900 240 280 45 35 460 80 40 150

According to the contemporary concepts of microbiologists and hydrologists, bacteria play a significant role in the nutrition of zooplanktonic organisms and zooplankton is regarded as one of the main items in fish nutrition. Taking into consideration the interactions of planktonic communities, bacteria are generally considered as a significant component in plankton nutrition networks that play a key part in biochemical cycles (Langenheder and Jürgens, 2001). The results of zooplankton investigations in Damietta Branch of River Nile are represented in figure (4), the overall average of total zooplankton detected at the study area was 547 .103 Ind. m ̶ 3. It increased in Benha station that recorded a seasonal average of 1095 .103 Ind. m ̶ 3 and the least zooplankton density was detected at Talkha and El-Serw stations (Fig. 4). The scarcity of zooplankton species at these two sites could be due to receiving of industrial waste at the first site and domestic and sewage effluents at the second. Zooplankton populations recorded during the present study were clearly dominated by Rotifera (80.8%) and Protozoa (13.5%), while crustacean zooplankton including cladocerns and copepods formed only 5.3 % of the total population (Fig. 5). The results of the present study on zooplankton community generally confirm to the hypothesis of similar community structure of zooplankton in rivers as postulated by Pace et al (1992). Zooplankton in fresh water rivers are often dominated by small forms such as rotifers and ciliates, bosminids and juvenile copepods throughout the year, with no marked development of the large bodied cladoceran and calanoid populations as in the case of the present study. Rotifera abundance differed among seasons, the seasonal pattern of rotifer variation and distribution is similar to that of total zooplankton. The highest peak of Rotifera was detected in spring (3542 .103 Ind. m ̶ 3) where the dominant species was Keratella cochlearis accounted for about 44% of the total rotifer abundance. Rotifera total density decreased to 1378 and 1486 .103 Ind. m ̶ 3 in the next summer and autumn seasons respectively, before it increased again in winter to 2430 .103 Ind. m ̶ 3. Negative weak correlation was observed between K. cochlearis and total bacterial count (r = - 0. 303) in Damietta Branch of River Nile during the present study. Feeding experiments with fluorescent microspheres and direct observation of living individuals indicated that K. cochlearis fed mainly on bacteria that were planktonic or attached to particles, and also on detritus ( Holst et al., 1998). Keratella cochlearis described as an important consumer of bacteria (Ooms-Wilms et al., 1995). Also, Keratella was the most common and abundant bacterivorous rotifer at the offshore site of Lake Erie, USA (Hwang and Heath, 1999). Winter peak of rotifers was dominated by polyarthra vulgaris which formed about 30% of total rotifers count. El-Shabrawy (1996) reported that temperature boosts the abundance of some zooplankton and causes the disappearance of the others. No correlation was found between water temperature and Rotifera density in Damietta Branch during the study. Khalifa (2000) revealed that there was a highly significant negative correlation between rotifers population density and water temperature (r = - 0.763, P >0.001) in the study of zooplankton communities in certain sites of River Nile receiving industrial wastewater. Electric conductivity revealed a moderate positive relation with both total bacteria count and bacterial biomass (r = 0.594 and r = 0.588), while no relationship was detected between the two zooplankton groups (Rotifera and Protozoa) and electrical conductivity. A weak negative correlation was detected between total dissolved solids and the two main zooplankton groups (Rotifera and Protozoa) in Damietta Branch of River Nile. The biomass and productivity of rotifers in Coqueiral Lake were inversely related to suspended matter (Casanova, 2009). According to Carvalho (1983), suspended particles may act on zooplankton in different ways. The large amount of suspended matter may obstruct zooplankton respiratory and swimming apparatuses and reduce light penetration, and thus phytoplankton productivity.

2684 J. Appl. Sci. Res., 8(5): 2679-2688, 2012

Fig. 4: Total zooplankton densities (Ind. 103 10-3) at the selected sampling sites of Damietta Branch.

Fig. 5: Percentage abundance of different zooplankton groups at the selected sites of Damietta Branch during the study period (Spring 2008-Winter 2009).

In the present study a strong negative correlation (r = - 0.964) was detected between total bacterial counts and rotifers density when it attained its maximum occurrence during spring (Fig. 6). While in the other seasons a positive moderate relationships revealed (r =0.482, 0.497 and 0.518 for summer, autumn and winter respectively). Hwang and Heath (1999) observed at coastal and offshore sites of Lake Erie that rotifers were usually more important bacterivores than cladocerans. Rotifers have been found to be the dominant grazers in other ecosystems, including freshwater estuaries in the USA (Havens, 1994), marine estuaries in Germany (Arndt and Heerkloos, 1989) and small eutrophic lakes in France (Lair and Ali, 1990), although sometimes this is not the case (Christoffersen et al., 1990). Negative weak relationships were found between rotifers standing crop and total coliforms, faecal coliforms and faecal streptococci where r = -0.308, -0.355 and -0.221, respectively. Since a highly positive correlation was detected between total Rotifera and total Protozoa (r = 0.838), protozoans follow rotifers in its relations with bacterial indicators except that it showed weak negative relationship with total bacterial count in summer (r = - 0.451) as shown in figure (7). Some studies in freshwater environments have demonstrated that protozoa (flagellates and ciliates) could be the major grazers of bacteria (Beaver and Crisman, 1989; Sanders et al., 1989).

2685 J. Appl. Sci. Res., 8(5): 2679-2688, 2012

Among crustacean zooplankton, cladoceran density (seasonal average 98 .103 Ind. m ̶ 3) was about two folds higher than copepods density (seasonal average 48 .103 Ind. m ̶ 3). The highest cladoceran standing crop was observed in autumn and its minimum values in summer. In contrast, maximum values of copepods were observed in summer and decreased to its least densities in spring and autumn. No relationships were displayed between cladocerans and total bacterial count during the study period except in spring when Cladocera showed strong negative correlation (r= -0.805) with it. Small cladoceran Bosmina longirostris was the dominant species in Damietta Branch in spring; it formed about 67 % of the total cladoceran count. Kim et al. (2000) observed that B. longirostris was a dominant grazer of bacteria in the Nakdong River, but it did not appear to graze at a rate that would significantly control the bacterial community. A similar result was found in Dutch lakes, where B. longirostris and B. coregoni were the most important grazers (Gulati et al., 1991). Also copepods was negatively correlated (r = -0.827) with total bacterial count in spring, while it had a positive relation (r = 0.835) in next summer, although nauplii were the dominated copepods in both seasons as it formed 89 and 98 % of the total group in spring and summer, respectively. The significance of copepod bacterivory was difficult to quantify because cyclopoids never appeared to be bacterivorous, while some nauplii and calanoid copepods were bacterivorous (Hwang and Heath, 1999). Also, indirect Bacterivory, i.e. copepod feed on protists that have consumed bacteria, may be significant (Hwang and Heath, 1997). Microzooplankton (rotifers and nauplii) played a more important role in grazing bacteria and phytoplankton than do macrozooplankton (cladocerans and copepods) in the lower Nakdong River (Kim et al., 2000). Hwang and Heath (1999) mentioned that, no one group of planktonic bacterivores dominated whole bacterivory at all times nor did any group show negligible bacterivory at any time. The study also found that community bacterial grazing differs from others in showing a greater importance of zooplankton (especially microzooplankton) bacterivory.

3 -3 6 Fig. 6: Seasonal variations in total Rotifera density (Ind.10 m ) and total bacterial count (TVBCs.10 CFU ml-1) in Damietta Branch of River Nile.

2686 J. Appl. Sci. Res., 8(5): 2679-2688, 2012

3 -3 6 Fig. 7: Seasonal variations in total Protozoa density (Ind.10 m ) and total bacterial count (TVBCs.10 CFUml -1) in Damietta Branch of River Nile.

Conclusions:

Zooplankton populations in the current investigation were dominated by Rotifera and the results indicated that there is a predominantly opposite relationship between total bacterial count and rotifers in spring when it attained its maximum occurrence, based on a prey- predator relationship in fresh water ecosystem. Also, rotifers were dominated by Keratella cochlearis, which has a weak negative correlation with the total bacterial count. In addition, the indicator bacteria exceeded the acceptable level at some sites, which revealed that Damietta Branch waters subjected to sewage pollution. A future task will be to identify Rotifera species that efficiently ingests bacteria in Branch of River Nile.

Acknowledgements

The authors are most grateful to Inland Water and Aquaculture Branch, National Institute of Oceanography and Fisheries, Cairo, Egypt which funded this work through a project entitled "Performing an Integrated Scientific System to Protect River Nile from Pollution and Developing its Fish Resources".

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