Estuaries and Coasts (2008) 31:1130–1142 DOI 10.1007/s12237-008-9102-3

A Preliminary Survey of the Nitrogen and Carbon Isotope Characteristics of from the Lagoons of ’s Delta

Autumn Oczkowski & Scott Nixon & Steve Granger & Abdel-Fattah M. El-Sayed & Mark Altabet & Richard McKinney

Received: 26 June 2008 /Revised: 13 August 2008 /Accepted: 23 September 2008 /Published online: 17 October 2008 # Coastal and Estuarine Research Federation 2008

Abstract The present study reports nitrogen and carbon probable importance of autochthonous particulate organic stable isotope data (δ15N and δ13C) from four large (63– matter rather than terrestrial detritus or marine plankton in 400 km2), shallow (∼1 m) coastal lagoons on Egypt’s Nile the diets of resident fish populations in the lagoons. Delta. While the lagoons all receive sewage and agricultural drainage, the magnitude of loading varies. In this prelim- Keywords Stable isotope . Nitrogen . Carbon . Egypt . inary survey, we document wide variability in the δ15N and Lagoons . Nile delta δ13C isotope values of major fish groups among these lagoons. There were no consistent or significant differences among the major groups of fish, including carp, catfish, Introduction mullet, and . There was a strong positive correlation (R2=0.84) between the average δ15N values of fish muscle Egypt’s Nile Delta is a highly engineered system that has and estimated water residence time among the lagoons. been modified by human activity for 5,000 years (Brewer This preliminary evidence suggests that nitrogen cycle 2005). Four large lagoons along the northern coast are transformations may be more important than primary N striking features on the delta landscape (Fig. 1). The source differences in determining N isotopic ratios of lagoons have an equally long history of human impact set organisms in the lagoons. The δ13C results point to the in the context of rapidly changing social and natural systems. Some of the modern pressures include the A. Oczkowski (*) : S. Nixon : S. Granger conversion of lagoon area to land agriculture, aquaculture Graduate School of Oceanography, University of Rhode Island, ponds and salt pans, changes in hydrology, circulation and South Ferry Road, sediment load, the addition of large amounts of agricultural Narragansett, RI 02882, USA e-mail: [email protected] drainage water and urban sewage, and dramatic increases in inorganic nutrient concentrations (Hamza 2006; Oczkowski A.-F. M. El-Sayed and Nixon 2008). There is also a long history of intensive Department Oceanography, Faculty of Science, artisanal fishing in the lagoons (Oczkowski and Nixon Alexandria University, Alexandria, Egypt 2008). The impacts of these pressures on the lagoon ecosystems are largely undocumented. M. Altabet While subjected to a range of ever-changing physical The School for Marine Science and Technology, and chemical conditions, the lagoons have generally University of Massachusetts Dartmouth, 706 South Rodney French Boulevard, remained productive. Together, they supply approximately New Bedford, MA 02744, USA 30% to 40% of Egypt’s commercial fish landings and provide an important local food source (GAFRD 2007). R. McKinney Anthropogenic sources of nutrients are sufficiently large Atlantic Division, US Environmental Protection Agency, 27 Tarzwell Drive, that at least part of this coastal fishery may be supported by Narragansett, RI 02882, USA nutrient loading from fertilizers and sewage associated with Estuaries and Coasts (2008) 31:1130–1142 1131

the agricultural practices on the delta and cities discharging sewage (largely untreated) either upstream or directly into the lagoons (Nixon 2003; Oczkowski and Nixon 2008). However, direct evidence that anthropogenic nutrients contribute to lagoon food webs and productivity is lacking. The agricultural drainage water also potentially links food chains in the lagoons to nutrients and terrestrial detritus from the highly productive agricultural vegetation covering the delta.

Context of the Study

With Egypt more than 95% desert, all of the nation’s agriculture and 90% of its population is confined to the narrow banks of the Nile and the delta (25,000 km2; Fig. 1; Nixon 2003). The delta itself is a complex mosaic of cities, towns, and villages set among large agricultural areas. Few of these small urban centers are equipped with sewage treatment infrastructure, and their waste is released into more than 13,000 km of drainage canals which eventually discharge to four large (63–500 km2), shallow (∼1 m deep) coastal lagoons (Burullus, Edku, Manzalah, Maryut) or directly offshore (Richards 1982; National Water Resources Plan 2017 2005). As water is such a valuable resource in Egypt, there are very dense and highly engineered networks of agricultural canals taking water from the Nile to irrigate tile-drained fields and agricultural drains to carry water from the fields for ultimate discharge to the lagoons or on the Mediterranean Coast (Stanley 1996; National Water Resources Plan 2017 2005). Since the closure of the Aswan High Dam in 1965, Egypt’s fertilizer consumption has increased almost four- fold, and the country’s population has more than doubled (FAO 2008). These changes suggest a dramatic increase in the N and phosphorous (P) loads to the delta ecosystem as ’ Fig. 1 The top panel: Egypt s Nile Delta with agricultural areas the amounts of agricultural runoff and sewage have indicated in grey (source data, Digital Chart of the World (DCW), Environmental Systems Research Institute, Inc. (ESRI) 1:1,000,000 continued to increase (Nixon 2003). The control of the scale). The Nile flows north through Cairo and then splits into the Nile also made it possible to provide irrigation all year and Rosetta and Damietta branches (black lines). Dark gray lines represent maintain the agricultural areas of the delta in almost some of the major drains and canals on the delta (data from DCW). continuous production. The crosshairs in the center of the image correspond to 31°0′ E, 31°0′ N. Lagoon panels (below top panel), clockwise from upper left, show Our purpose in this preliminary study was to take Burullus, Manzalah, Edku, and Maryut lagoons. Sampling locations advantage of two opportunities to visit the delta lagoons and are represented by closed circles, and the fish collected at these obtain samples of common commercial from each locations are identified in Table 4 and correspond to the identification system. No stable isotope measurements have been reported numbers associated with the circles. In Maryut Lagoon, only the Main Basin (MB) and Fisheries Basins (FB) are shown. The Desert Road from the lagoons, and we hoped that stable isotopes would divides these two basins and fish, water, and Nile lily samples were prove useful in documenting human influences on food webs taken from each basin (at the closed circles). The city of Alexandria and productivity in this very complex and perturbed environ- lies between Maryut Lagoon and the Mediterranean Sea. A sample of ment. We also sought to evaluate the importance of commercial fish food was sampled near Manzalah Lagoon at the closed circle labeled FF anthropogenic inputs compared to in situ N transformations in determining differences in nitrogen isotope values (δ15N) in lagoon food webs and to investigate the potential importance of terrestrial C and fresh and brackish water phytoplankton C sources in lagoon food chains. 1132 Estuaries and Coasts (2008) 31:1130–1142

Stable isotopes are now commonly used to look at the and particulate N of 1–2‰ (Sheats 2000). It was unclear at impact of anthropogenic nutrients on biogeochemical the outset if δ15N of fish from the different lagoons would cycles and food web structures (e.g., McClelland et al. be distinguishable or much greater than about 4–5‰ 1997; Fry 2002; Rogers 2003; Savage 2005; Oczkowski et (allowing for trophic fractionation of 3–4‰ from primary al. 2008). This is possible because N introduced via human producers). However, N isotopes fractionate with in-stream activities such as sewage effluent and fertilizer application, uptake, nitrification, and denitrification, and the δ15N can often be distinguished from N supplied by “natural” values observed in biota represent a complex mix of both sources (Fry 2006). Differences in the isotope ratio of heavy source and in-stream processing. Fry and Allen (2003) carbon (13C) to light (12C) in terrestrial plants and phyto- observed bivalves with δ15N values consistently >10‰ in plankton have been used for over 40 years to assess the the Mississippi River, which drains a large agricultural relative importance of terrestrial plant detritus compared with watershed. Raw wastewater (δ15N about 2‰ and 6‰, for − + in situ plankton primary producers in influencing secondary NO3 and NH4 , respectively) retained in temperate ponds productivity in coastal marine ecosystems (Parker 1967; for 13–20 days also had δ15N>10‰, which also points to Haines 1979;Fry2006). Numerous studies have shown that the significance of in situ fractionation ( et al. 1997). different sources can be discerned even without character- Considering the complex network of agricultural drains on ization of the specific sources (Schlacher et al. 2005; Vizzini the delta, it seemed possible that fractionation of δ15Nin et al. 2005; Abreu et al. 2006; Bannon and Roman 2008; the bioavailable N pool would take place during transport Oczkowski et al. 2008). and fish would be characterized by much heavier (>10‰) We chose to focus primarily on the stable isotope values isotope values (Stanley 1996). of fish because they are of great commercial interest and are We anticipated that the contrast between δ13C source relatively long term integrators of nutrient enrichment and values would be more distinct, as fractionation within the carbon sources supporting secondary production (Vizzini et food web is far less for δ13C (Fry 2006; Finlay and Kendall al. 2005). 2007). Mediterranean fish typically have δ13Cvalues It was our hypothesis that differences in flow rates, crop ranging from −9‰ to −20‰ (Vizzini et al. 2002; Azzurro types, fertilizer demands, and different levels of sewage et al. 2007), while freshwater phytoplankton typically range enrichment would be reflected in the isotope composition from −32‰ to −23‰ (Finlay and Kendall 2007). There are 13 of primary producers and consumers in the Nile Delta some C4 plants with δ C values similar to marine lagoons. However, fertilizers and nitrogen-fixing crops phytoplankton grown on the delta (e.g., maize, δ13C≈ 15 (berseem, rice) have δ N values of about 0‰ (Aly et al. −13‰), but most agricultural plants in this system have C3 1982;Fry2006), and these N sources might not be metabolic pathways and δ13C within the range of freshwa- distinguishable from the Mediterranean, where surface ter algae (Fry 2006). Virtually all of the non-urban land on particulate organic nitrogen is also on the order of 0‰ the delta is cultivated. (Pantoja et al. 2002). While secondary- or tertiary-treated sewage frequently has a δ15N value much heavier than The Nile Delta Lagoons 10‰ (McClelland et al. 1997; Savage and Elmgren 2004), this may not be true for the raw or primary sewage found in The four coastal lagoons on the Nile Delta, Burullus, Edku, Egypt. Primary effluent may have δ15N values of ammo- Manzalah, and Maryut, support more than 30% of Egypt’s + − nium (NH4 ) on the order of 6–7‰,NO3 of about 3‰, total commercial fish catch (Table 1;GAFRD2007).

Table 1 Some characteristics of the Nile Delta lagoons

Lagoon Sizea (km2) Salinitya Fish landingsb Agricultural drainage inflowc Direct sewage inflowc (103 mt) (109 m3 year−1) (109 m3 year−1)

Burullus 500 ∼2–20 53.9 4 – Edku 71 ∼2–20 9.6 2 – Manzalah 450 3–40d 39.9 7 – Maryut 63 2–5 5.3 0.3 0.33–0.37

All direct sewage and agricultural drainage data are from various measurements made in the 1990s and all of the lagoons are ∼1 m deep a From El Shenawy 1994; EA Engineering 1997; Dewidar and Khedr 2001; Okbah and Hussein 2006; Oczkowski and Nixon 2008 b Data from 2005 (GAFRD 2007) c From Samman 1974; Abdel-Moati and El-Sammak 1997; Khalil 1998; El-Sherif and Gharib 2001; Abdallah 2003; El-Rayis 2005; Al Sayes et al. 2007 d In September 1995, when the highest salinity was found near the breachway and the lowest inshore Estuaries and Coasts (2008) 31:1130–1142 1133

Maryut Lagoon, just inshore of the city of Alexandria, is gradients from high values near the breachway to the most highly engineered. Since the 1960s, its area has brackish inshore (Table 1;El-Shenawy1994;Dewidar decreased rapidly due to filling, urbanization, and the and Khedr 2001; Okbah and Hussein 2006). Maryut has construction of dykes for fish farms and salt pans. It has salinity in the range of 2 to 5 psu (EA Engineering 1997). also been divided into four separate basins, all of which Inorganic nutrient concentrations (DIN, DIP) in the receive agricultural drainage. Beginning in the 1980s, lagoons also show gradients with greatest concentrations Alexandria’s primary treated and raw effluent (today ∼9– near the agricultural drains or sewage discharge points 10×105 m3 day−1) has been discharged into the main basin, (EA Engineering 1997;Shakweer2005; Shakweer 2006; coincident with a precipitous decline in the fishery (EA Al Sayes et al. 2007). Maryut’s main basin is most Engineering 1997; Oczkowski and Nixon 2008). While enriched, with DIN at least one order of magnitude Maryut is the only lagoon that receives a sizeable amount higher than the other lagoons (Table 2;EAEngineering, of direct sewage, Manzalah Lagoon ultimately receives 1997;ElRayis2005). Recent nutrient data for Edku about 65% of Cairo’s sewage and industrial effluent (Samir lagoon are inconsistent (Table 2), perhaps due to spatial 2000). The waste from Cairo is first discharged into an heterogeneity. agricultural drain that transports it approximately 100 km to We hoped to capture seasonal differences in the the southeast corner of Manzalah Lagoon (Samir 2000). hydrology and agriculture in our sampling. During the All four lagoons receive substantial, albeit varying, Egyptian winter (November to May), flow from agricultural amounts of agricultural drainage water, which is their only drains is roughly half that of summer (El Atfy et al. 1991; freshwater input (Table 1). The drainage is a complex mix Roest 1999; El-Sayed 2007). Summer (May to October) is of runoff from fields, adjacent fish farm effluent, industrial the high growing season with maize, rice, cotton, and effluents, and raw or partially treated sewage from cities sugarcane making up about 60% of the total summer and villages on the delta. The nutrient loads vary with cropping land of 2.48×106 ha (El Sayed 2007). Berseem location and season, depending on what crops are being (Egyptian clover, Trifolium alexandrinum) and wheat are grown upstream, the influence of fish farms, and the the major winter crops accounting for 40% of the growing importance of local sewage and industrial effluents. area (Skold et al. 1984;Attia2004; El-Sayed 2007). Drainage water may also be reused for agriculture and Vegetables are grown throughout the year. The summer aquaculture many times. crops have much higher nitrogen fertilizer requirements Only Maryut Lagoon lacks a direct connection with than do winter crops, often resulting in a fertilizer shortage the sea, and the open systems show strong salinity during summer (El-Sayed 2007).

Table 2 Recent (post 1990) nutrient concentration data from the delta lagoons

− Year sampled Mean annual DIN (μM) Mean annual PO4 (μM) Frequency Number of stations Reference

Burullus 2000 2a 2 Monthly 15 Radwan 2005 2002 15b 3c Seasonally 15 Al Sayes et al. 2007 2003 20 2 Seasonally 11 Okbah 2005 Edku 1992 70 <1 Seasonally 5 El-Shenawy 1994 1999–2000 90 8 Seasonally 10 Abbas et al. 2001 2000 50 10 Seasonally 10 Okbah and El-Gohary 2002 2004 3 <1 N.A. 10 Shakweer 2006 Manzalah 2001 14 3 Bimonthly 9 Shakweer 2005 Maryut 1991–1992 1850 57 Annual average N.A. EA Engineering 1997 1992–1993 770 190 Annual average N.A. EA Engineering 1997 1995–1996 590 207 Monthly 3 EA Engineering 1997 N.A. 590 56 N.A. 14 El-Rayis 2005

N.A. information not available a − Just NO3 b − + − NO2 and NH4 data were presented as seasonal averages for each station, and we averaged these to obtain a mean for the lagoon. NO3 data were not available in tabular form and, thus, were approximated from seasonal contour plots c PO4 data were approximated from seasonal contour plots from 2001 as 2002 data were not presented 1134 Estuaries and Coasts (2008) 31:1130–1142

The Coastal Lagoon Fish (Froese and Pauly 2007). Carp are omnivorous freshwater fish with different species specific diets consisting of a wide The most abundant fish in the Nile delta lagoons are tilapia range of plants and detritus as well as crustaceans and and a few other species with wide environmental tolerances mollusks (Table 3; Froese and Pauly 2007). and flexible feeding habits (Table 3). Tilapia are herbivo- rous or omnivorous, with feeding habits that often change diurnally or with season (Table 3; El-Sayed 2006). There Materials and Methods are four tilapia species present in the lagoons, but the Nile Tilapia (Oreochromis niloticus) is the most abundant Fish and Plants (Table 3; Toews and Ishak 1984; Shakweer and Abbas 2005; Al Sayes et al. 2007). Over 120 fish were obtained from 18 fishermen and nine Mullet, catfish, and (to a lesser extent) carp also local markets during November 2005 and August 2006 contribute in a small way to the commercial landings from (Fig. 1). Their provenance was determined through inter- the lagoons (Table 3; Al Sayes et al. 2007; Toews and Ishak preted interviews. Where possible, we purchased (or, more 1984). All of the mullet species have similar feeding habits frequently, were given) fish directly from fishermen in the (Table 3). There are two main species of catfish in the field. The fish from small outdoor markets were obtained in lagoons: Bayad (Bagrus bayad) and what is locally called villages on the edges of the lagoons. Karmout (Clarias lazera; Table 3). Both are omnivorous Specimens were numbered and photographed for later and feed slightly higher on the food chain than tilapia and use in identification to genus and, occasionally, species. A mullet (Adham 2002; Froese and Pauly 2007). The catfish portion of tail muscle from each fish was removed, dried at are freshwater species that are tolerant of brackish environ- 65°C for 48 h and kept in individual plastic bags filled with ments, as well as a wide range of environmental conditions non-iodized salt for transport back to the University of

Table 3 Common commercially important fishes in the Nile Delta lagoons

General Species commonly found in Egypt Feeding habits Selectivity name

Tilapiaa Nile tilapia (Oreochromis niloticus) Phytoplankton, zooplankton, detritus Low Blue tilapia () Phytoplankton, zooplankton, detritus, Some food preferences residues Redbelly tilapia (Tilapia zillii) Macrophytes, blue-green and green algae, detritus, Plant over , seasonal zooplankton, insects and larvae, diatoms, rotifers, variability benthic invertebrates, arthropods Galilee tilapia (Sarotherodon galilaeus) Dinoflagellates Very high Mullet Thinlip mullet (Liza ramada)b Epiphytic algae, detritus, small benthic or planktonic organisms, eggs, larvae Gray mullet (Mugil cephalus)b Zooplankton, detritus, benthic organisms, algae Mainly algae in fresh waters Leaping mullet (Liza saliens)c Zooplankton, detritus, periphyton, small benthic organisms Golden Grey Mullet (Liza auratus)b Small benthic organisms, detritus, and occasionally insects and plankton Catfish Bayad (Bagrus bayad)b Small fish, insects, crustaceans, mollusks, plants Adults are piscivorous Karmout (Clarias lazera)d Omniverous, scavenger Prefers benthic organisms and detritus Carp (Ctenopharyngodon idella)b Plants, detritus, insects, invertebrates Prefers plants (Aristichthys nobilis)b Mainly zooplankton (Cyprinus carpio carpio)b Insects, crustaceans, annelids, mollusks, seeds, aquatic plants and algae Nile carp ( niloticus)e Plants, detritus, small Juveniles prefer phytoplankton a Summarized from El-Sayed (2006) b Information on feeding habits from Froese and Pauly (2007; www.fishbase.org) c Fernandes et al. (2007) d Adham (2002) e El Moghraby and El Rahman (1984) Estuaries and Coasts (2008) 31:1130–1142 1135

Rhode Island (URI). The samples were redried in the Water samples were also analyzed for δ15N in nitrate − − + laboratory and all fin, skin, and bone carefully removed. (NO3 ), nitrite (NO2 ), and ammonium (NH4 ) using both a The muscle flesh was ground to a fine powder with a nitrous oxide method (McIlvin and Altabet 2005) and the mortar and pestle and stored in acid washed scintillation ammonium diffusion method at the Marine Biological vials in a desiccator until analysis. Laboratory, Woods Hole, MA, USA (Sigman et al. 1997). Samples of the Nile Lily or Water Hyacinth (Eichhornia The nitrous oxide method has the advantage of determining 15 − − crassipes), a vascular floating plant, were also collected from δ N values of the NO3 and NO2 separately, while the the main and fisheries basins of Maryut Lagoon (Fig. 1). A ammonium diffusion method measures these forms togeth- 15 + sample of commercial fish feed was obtained from a local er. The δ N value of NH4 for the Main Basin of Maryut fish farmer (Fig. 1). Lily samples comprising multiple leaves Lagoon was also determined commercially via ammonium and stems were dried, and they and the fish feed were diffusion. ground and stored in the same manner as the fish. The carbon and nitrogen stable isotope values were Data Grouping and Statistical Analyses determined using a Carlo-Erba NA 1500 Series II Elemental Analyzer interfaced with a micromass optima mass spec- Presenting and discussing the results required that we trometer with a precision of better than ±0.3‰ at the US develop a specific terminology that reflects the way in Environmental Protection Agency (EPA) Atlantic Ecology which data were grouped. While one might assume that Division in Narragansett, Rhode Island. The carbon isotope results should be presented by species, most of the fish composition was expressed as a part per thousand (permil) could not be identified to species level. For example, tilapia deviation (δ13C ‰) from the reference standard PDB, and classifications are continuously changing, and the different nitrogen isotope composition (δ15N ‰) was expressed as a species in the lagoons appear very similar and often part per thousand (permil) difference from the composition hybridize (El-Sayed 2006). Since our classifications were of N2 in air (Mariotti 1983) as follows: only good to the genus, we reported results for general ÂÃÀÁ groupings of fish (tilapia, catfish, mullet, carp). We defined dX ¼ R R 1 103 sample standard “group average” as the mean of all fish of a group (tilapia, where X is δ 13Corδ15N and R is the ratio 13C/12Cor catfish, mullet, carp) sampled at a specific location and 15N/14N. Samples were analyzed randomly, and in dupli- date. When fish of the same group were purchased from cate, in batches of approximately 25. We used laboratory separate stalls within a marketplace or from different standards to check for instrument drift in each run; no drift fishermen fishing in different places in the same lagoon, was observed in analyzing the samples discussed here. they were treated as separate groups. Lagoon means are the mean of all of the individual fish of all groups collected Water from that particular lagoon during a particular season (August 2006 for all lagoons as well as November 2005 Two water samples from Maryut Lagoon were collected for Manzalah). As only fish from Manzalah Lagoon were during August 2006 at the same time and place where the sampled in November 2005, and there may have been Nile Lily was collected. Approximately 1 l was taken just seasonal differences in the fish tissues, we only used data below the surface, preserved in the field (2 ml/l chloroform; from August 2006 in comparisons among lagoons. Nixon et al. 2007), and stored in a dark cooler with ice We used one way analyses of variance and a paired packs. Within 6 h of collection, the water was filtered Student’s t test to determine if different locations where fish through precombusted Whatman GF/F glass fiber filters were purchased, groups, and lagoons were significantly and stored in dark acid-washed polyethylene bottles for different from one another. When comparing isotope values transport to URI. Once in the laboratory (10 days after among lagoons to residence time and fish catch, we used collection), the samples were frozen until analysis for regression analysis to determine if the slopes of trends were nutrient concentrations and δ15N. significantly different from zero. All analyses were Nutrients (ammonium, nitrate, nitrite, and orthophos- performed using JMP (JMP Release 6.0.0 2005). phate) were analyzed using a Lachat Instruments Quik Chem 8000 flow injection analyzer (Lachat Instruments/ Hach, Loveland, CO, USA) at the Graduate School of Results and Discussion Oceanography using US EPA approved methods (see Nixon et al. 2007). Salinity was determined using an There was a very large range in the isotope ratios of optical refractometer and the Sargasso Sea water used for individual fish, with δ15N values ranging from 5‰ to 22‰ blanks and standard curves was adjusted, via dilution, to the and δ13C values from −30‰ to −9‰ (Fig. 2). Most of the salinity of the samples. fish in the lagoons had δ15N values far heavier than those 1136 Estuaries and Coasts (2008) 31:1130–1142

30 Freshwater Phytoplankton Mediterranean 11/2005 drainage water is a good indicator of the amount of Manzalah: & C Plants Fish 15 25 3 Tilapia δ Mullet nutrients reaching the lagoons. The N means seem 8/2006 inversely correlated with fishery yields per unit area of the 20 Burullus: Tilapia lagoons (Fig. 3). This correlation (albeit among only four Catfish N Edku: systems) may arise indirectly from correlations between

15 15

δ Tilapia Manzalah: area-specific fisheries landings and primary production 10 Tilapia Catfish (e.g., Nixon 1988; Iverson 1990) and between area-specific Mullet Maryut: N loading and primary production (e.g., Nixon 1992; 5 Tilapia Carp Boynton and Kemp 2000), where an excess of anthropo- δ15 0 genic nutrients (presumably with heavy N values) may -30 -25 -20 -15 -10 -5 contribute to decreased fisheries production (Oczkowski δ13C and Nixon 2008). But, our hypothesis is that N fraction- ation within the lagoons and drains contribute to the Fig. 2 All fish data for the Nile Delta Lagoons. Approximate ranges 13 differences observed in the fish. of δ C values for C3 plants and Mediterranean fish are shown with arrows (Fry 2006; Vizzini et al. 2002; Azzurro et al. 2007) In shallow freshwater lakes and reservoirs, as well as estuaries, N removal through denitrification can be high and approximately proportional to the water residence time typical of synthetic fertilizers (0‰), raw- or primary-treated (Howarth et al. 1996; Nixon et al. 1996; Seitzinger et al. sewage (≈3–7‰), offshore POM (≈0‰), and the commer- 2006). Denitrification can fractionate N isotopes, where the cial fish food sample (2‰), thus, documenting the denitrifying bacteria take up the lighter N isotope at a faster importance of N transformations and fractionation in the rate than the heavier, leaving the remaining bioavailable dynamic isotope landscape (Aly et al. 1982; Sheats 2000; DIN enriched in 15N (e.g., Lehmann et al. 2003). Thus, with Pantoja et al. 2002). In a study of four estuaries, Fry et al. increased residence time, we might see heavier δ15N values. (2003) found that the system with the most agricultural Because residence time values were not available for all drainage had the heaviest δ15N values and suggested that systems, we estimated residence times for the lagoons using temperature may have been an important factor in promot- the most recent water discharge and lagoon area (volume) ing microbial activity in the agricultural soils. Such activity data available (Samman 1974; EA Engineering 1997; could also promote nitrification and denitrification reac- Khalil 1998; El-Sherif and Gharib 2001). Our estimates tions, making the δ15N in the inorganic N loaded to these also show a positive relationship (Fig. 4). Using the systems heavier. The nonmigrating fish (i.e., groups other relationship between percent N retained and residence time than mullets) had δ13C values that clearly fell within the from a cross-systems comparison, we estimate that the two range of fresh or brackish algae and terrestrial (C3) plants systems with the longest residence times (about 45 days, rather than the range reported for other Mediterranean fish Burullus and Maryut) retain an estimated 85% of N inputs, (Fig. 2; Fry 2006; Vizzini et al. 2002; Azzurro et al. 2007). while the lagoon with the shortest residence time (8 days, Only highly migratory mullets, which move between inshore Edku) retains only half of this amount, or about 45% and offshore, reflected a fully marine food web. The (Nixon et al. 1996). relatively heavy N signal in the fish suggests that the light 18 C signal is due to the consumption of organic matter R2=0.8339 R2=0.0650 16 Maryut Maryut produced within the lagoons and drains rather than from P=0.09 P=0.75 14 Burullus terrestrial detritus. The widespread use of synthetic fertilizer Manzalah

N 12 15 Burullus δ 15 10 on the delta would lead to much lighter N values of crops. δ Edku Manzalah 8 Edku Comparisons Among Lagoons 6 4 80 100 120 140 160 180 200 2 4 6 8 10 12 14 16 18 13 While there were no differences in δ C, there were Catch per unit Area Drainage per unit area significant differences in δ15N values among lagoons. Fish (tons km-2) (106 m3 km-2 y-1) from Edku (δ15N of 7.96‰) were significantly (P=0.0461) Fig. 3 Mean (± Standard Error) δ15N in fish from each of the Nile lighter than Manzalah (11.73‰), and fish from Burullus Delta lagoons sampled during summer 2007 and plotted as a function and Maryut (13.01‰ and 14.10‰, respectively) were of fisheries landings in 2005 (left; GAFRD 2007) and agricultural statistically different from the other two lagoons but not drainage inflow normalized to lagoon surface area (right). Closed from one another. These differences were not correlated circles represent all fish and hollow circles are just tilapia. When the means of all of the data and just the tilapia are the same, or very with the amount of drainage water the lagoons received similar, only the hollow circles are visible. Regression lines, R2, and P (Fig. 3). However, we do not know if the volume of values are for all of the data Estuaries and Coasts (2008) 31:1130–1142 1137

R2 = 0.84 (all fish) Differences Among Taxonomic Groups 16 Maryut R2 = 0.90 (tilapia) 14 With the exception of mullets, there were no statistically 15 13 Manzalah significant differences in δ N and δ C among the various 12 taxonomic groups of fish. This may not be as surprising as

N Burullus it first seems, given that all of the groups are very general 15 Edku

δ 10 feeders with low selectivity. Unfortunately, sample sizes

8 within lagoons were too small to make within lagoon comparisons meaningful. However, the heaviest fish for 15 6 All Fish δ N were catfish from Burullus and Manzalah lagoons Tilapia (19.65‰ and 16.45‰, respectively; Table 4) and their 4 mean isotope values were 3.60‰ and 2.49‰ heavier than 10 20 30 40 50 the next highest samples from the two lagoons, consistent Residence Time (days) with the approximate 3.5‰ fractionation between trophic Fig. 4 Mean δ15N values for fish from each of the Nile Delta lagoons levels (Fry 2006). It is possible that these particular fish sampled during August 2007 and plotted as a function of our estimates of may reflect a more carnivorous diet as catfish are known to water residence time as described in the text. Error bars represent ±1 SE. consume small birds, fish, and rotting flesh (Froese and Regression line for all fish Pauly 2007). In November 2005, mullets purchased from two fishermen on Manzalah Lagoon had lighter δ15Nand heavier δ13C values than all other fish collected. These

Table 4 All fish collected during the two sampling periods and their mean isotopic values, standard deviations, and number of individuals collected

I.D. Common name Genus δ15N SD δ13CSDn

November 2005 Manzalah 6 Mullet Mugil sp. 5.08 2.99 −11.61 2.32 8 6 Mullet Mugil sp. 10.91 1.60 −24.15 4.51 3 6 Tilapia Tilapia sp. 15.56 1.46 −25.32 1.23 6 6 Tilapia Tilapia sp. 16.38 1.38 −26.14 0.45 14 6 Tilapia Tilapia sp. 14.89 1.29 −27.14 1.72 3 6 Tilapia Tilapia sp. 16.71 1.70 −26.48 0.35 7 August 2006 Maryut (main basin) 7 Tilapia Tilapia sp. 15.79 3.49 −25.78 1.96 6 Maryut (fisheries basin) 8 Carp Aristchthys nobilis 9.63 0.44 −24.40 0.43 4 8 Tilapia Tilapia sp. 15.20 2.48 −27.94 1.51 7 Edku 9 Tilapia Tilapia sp. 7.95 0.75 −25.59 0.72 4 Burullus 3 Catfish Clarias sp. 19.65 2.62 −26.89 0.25 3 1 Tilapia Tilapia sp. 13.40 1.61 −23.47 2.69 7 2 Tilapia Tilapia sp. 9.52 1.80 −25.37 1.84 6 3 Tilapia Tilapia sp. 16.05 3.43 −27.45 1.26 6 Manzalah 5 Catfish Clarias sp. 11.02 0.68 −29.90 1.22 3 6 Catfish Clarias sp. 16.54 1.23 −27.05 0.38 4 6 Mullet Mugil sp. 12.18 0.35 −25.73 1.19 6 4 Tilapia Tilapia sp. 13.35 2.14 −28.50 1.55 9 5 Tilapia Tilapia sp. 6.12 1.63 −23.61 4.85 6 6 Tilapia Tilapia sp. 9.55 0.67 −30.33 0.73 6 6 Tilapia Tilapia sp. 14.05 1.27 −27.49 0.31 6

The I.D. column refers to the locations where the fish were collected, which are identified in Fig. 1 1138 Estuaries and Coasts (2008) 31:1130–1142 mullets were also much more variable, with greater offer some preliminary encouragement that spatial variabil- standard deviations than the other samples, including ity within the lagoon may be discernable among consumers. mullets obtained in August 2006 (Table 4). Their carbon The Main Basin of Maryut Lagoon receives all of the values were more characteristic of δ13C values seen in city of Alexandria’s sewage effluent (primary treatment; EA offshore fish elsewhere in the Mediterranean, which can Engineering 1997). Because of the high pollution level, it is range from −9‰ to −20‰ (Jennings et al. 1997; Vizzini illegal to catch and sell fish from the Main Basin but and Mazzola 2006;Azzuroetal.2007). Our interpretation permissible to do so from the adjacent Fisheries Basin. is that the fish may have either recently migrated into Thus, we expected to find the average δ15N values in the Manzalah from offshore or that the source of the fish was Main Basin fish to be heavier than those from the Fisheries misidentified in the market. Mullets spawn offshore but Basin as sewage effluent is frequently, although not always, are known to spend significant portions of their lifecycle characterized by heavy δ15N values (Sheats 2000). Surpris- in estuarine and brackish waters (Blaber 1997). These are ingly, tilapia from the Main and Fisheries basins were the only fish in the dataset characterized by distinct nearly identical (15.79‰ vs. 15.20‰) but about 5.5‰ inshore or offshore migrations. heavier than carp from the Fisheries Basin (Table 4). In order to check the possibility that fish taken from the main Within Lagoon Variation (illegal) basin might have been misrepresented as having been caught in the fisheries basin, we collected Nile Lily Only the stable isotope values of fish collected from Burullus growing in each basin as well as water samples. As in the − Lagoon correspond in an obvious way with the spatial fish, the isotopic composition of the plants and NO3 were characteristics of the system. Tilapia with the lightest δ15N heavy and similar in both areas (Table 5). These data were purchased near the breachway (9.52‰), while the suggest that the adjacent basins may not offer such a heaviest were obtained about 7 km away, near large inputs dramatic contrast as previously thought. While DIN of agricultural drainage water (16.05‰). The heavy δ15N concentrations were also similar in the basins, the δ15N 13 − tilapia also had the lightest δ Cvalues(−27.45‰), value of the NO2 in water from the two basins was − consistent with freshwater POM and terrestrial C3 plant dramatically different (Table 5). The very heavy NO2 in material (Fry 2006). A similar pattern was observed in the main basin was associated with extraordinarily high − Mauguio Lagoon, in Southern France (Western Mediterra- NO2 concentrations (about 60 μM). Dominance of the 13 − nean), where fish were about 3‰ heavier in δ C and 0.5‰ DIN pool by NO2 is remarkable and must reflect a lighter in δ15N at a station near a breachway compared to particular pollutant source or very unusual conditions − another in close proximity to riverine inputs (Vizzini et al. within the basin. High concentrations of NO2 have been 2005). Those differences were attributed to differences in freshwater and marine N and C sources. In Burullus Table 5 Nutrient concentrations and δ15N values of Nile Lily − − Lagoon, however, plankton, either autochthonous or from (Eichhornai crassipes) and dissolved nitrate (NO3 ), nitrite (NO2 ), + drainage, are probably the main C sources as the fish also and ammonium (NH4 ) for the main and fisheries basins of Maryut Lagoon had heavy δ15N values. Plant detritus from agriculture has been heavily fertilized and the δ15N of its detritus is likely Maryut Lagoon Main Basin Fisheries Basin light. Contributions from nearby fish farms, which dis- charge into drains, are probably not an important source of Particulates Nile Lily (‰)1920 C either as the commercial feed has a value of about −20‰ 15 Nutrients and δ Nof2‰. − NO3 (μM) 76.03 112.18 δ13 − Tilapia in Burullus with the heaviest C values were NO2 (μM) 59.83 41.07 + collected along the north shore of the lagoon and west of NH4 (μM) 5.30 1.74 3− μ the other stations, about 23 km west of the breachway PO4 ( M) 3.37 1.16 (-23.47‰; Fig. 1). This part of the lagoon also had the Chemical method δ15 − ‰ highest pH values overall and chlorophyll-a values higher N, NO3 ( ) 20.82±0.74 21.64±0.08 δ15 − ‰ than near our other stations in a 2003 survey (Okbah and N, NO2 ( ) 33.98±0.65 7.31±0.05 13 Diffusion method Hussein 2006). The heavier δ C values may be reflecting 15 − δ N, NO3+2 (‰) 31.43 14.69 greater productivity in this portion of the lagoon associated 15 + δ N, NH4 (‰) 16.80 with dissolved inorganic carbon (DIC) demands and δ15 − − available DIC forms at a higher pH (Finlay and Kendall The NinNO3 and NO2 were determined separately using the 2007; Oczkowski et al. 2008). While these correlations are nitrous oxide analytical method (chemical, McIlvin and Altabet 2005) while the ammonia diffusion method (diffusion) determined the δ15 N + − − speculative and based on coarse sampling (we know only value of NH4 and of NO3 and NO2 combined. Samples were the general location from which fish were caught), they do collected in August 2006 Estuaries and Coasts (2008) 31:1130–1142 1139 observed in fish ponds and aeration lagoons at sewage matter have been observed in the US (Ohio River), with treatment plants. Such cases have been attributed to cooler fall δ13C values also heavier than summer (−21‰ vs temperatures (below about 17°C), herbicides, large temper- −25‰), which the authors attributed to changes in river- ature fluctuations, or low oxygen conditions (Durborow et flow and seasonal dominance of different phytoplankton al. 1997; Rich 2003). The first two do not apply in this case and C3/C4 plants (Munson and Carey 2004). as summer temperatures are far greater than 17°C, and herbicides have little impact on the system (EA Engineering − − 1997). When the oxidation of NO2 to NO3 occurs more Conclusions + − slowly than the oxidation of NH4 to NO2 or, in low − − 15 oxygen systems, the reduction of NO3 to NO2 occurs The mean δ N values of fish from the lagoons corre- − − more rapidly than denitrification (NO2 to N2), NO2 can sponded well with estimated water residence times, where build up and become toxic to fish (Durborow et al. 1997; the lagoons with the longest residence times had the − 15 Rich 2003). These high NO2 concentrations may have heaviest δ N values. It is not surprising that Maryut had contributed to the decline in fisheries landings seen in the heaviest δ15N values of the four lagoons as it no longer Maryut Lagoon since the late 1970s (from 200 to 60 tons has open exchange with the sea and receives a very large km−2; Oczkowski and Nixon 2008). amount of minimally treated sewage. As we were only able to sample fish from one location in The δ13C values of the fish were similar to freshwater Edku Lagoon, we were not able to evaluate spatial phytoplankton and agricultural detritus. The only exception variability. We collected six different group samples from was mullet from November 2005 that had both δ13C and one location in Manzalah Lagoon in November 2005 and δ15N values similar to the Mediterranean. Mullets are the seven different group samples from three different locations only fish in the dataset that are catadromous (Blaber 1997; in August 2006 (Table 4). However, there were no Froese and Pauly 2007). While δ13C values of detritus and observable patterns in the data. Manzalah Lagoon has more freshwater plankton are the same, freshwater phytoplankton than 1,000 islets that divide the lagoon into about 30 basins are probably a more important food source for the fish (Shakweer 2005), and the fish may simply reflect the (carp, catfish, tilapia) than terrestrial detritus, as the light spatial heterogeneity of this lagoon and poor mixing and δ13C values are coupled with heavy δ15N and agricultural circulation of the water. detritus would probably have δ15Nvaluescloserto synthetic fertilizer and atmospheric N (∼0‰). Differences Between Seasons In this highly complex metabolic system, it is not surprising that N transformations within the lagoons and We were only able to sample one of the lagoons (Manzalah) drains appear to be more important in influencing the fish during the different seasons. The mean N and C isotope δ15N values than the original sources, which are all values of the strictly inshore fish from Manzalah Lagoon (i.e., isotopically light (fertilizer, minimally treated sewage, and excluding mullets) were significantly heavier during No- the Mediterranean Sea). With the exception of some mullet, vember 2005 than in August 2006 (δ15N, P<0.0001; δ13C, the δ15N values of the fish ranged from 5‰ to 25‰. These P=0.0100). The mean δ15N value from November was values may be related to processes such as denitrification enriched by 4.49‰ over August (16.14‰ vs. 11.65‰), and biological uptake during both drainage transport and but the differences in δ13C values were slightly less within the lagoons, as has been suggested by the link (−26.15‰ vs. −27.71‰;Table4). These differences may between residence time and heavier δ15N values. The δ15N reflect seasonal regimes. Summer flow from agricultural values cannot be used to determine the anthropogenic drains is double that of winter, and fertilizer use is also nutrient contributions to the lagoonal fisheries, but com- much greater (El Atfy et al. 1991;Roest1999;El-Sayed bined with δ13C, we can gain some insight into the relative 2007). The summer residence time of water in these drains importance of pollution sources and N processing in these and lagoons is likely shorter than in winter, and less time ecosystems. for N processing may lead to lighter δ15N values during the summer. Also, the fish from the summer may have Acknowledgments We thank Youssef Halim, Soha Hamede, Edward Merchant, Amy Van Keuren, Betty Buckley, Lin Zhang, and consumed more plant material produced from synthetic 15 Taixing Wu for their help in sample collection, preparation, and fertilizer from the drains, which would lead to lighter δ N analysis and two anonymous reviewers for their thoughtful comments. values (Aly et al. 1982). Lower δ13C values in the summer This work was funded by a National Science Foundation (NSF) may be due to increased freshwater plankton abundance Biological Oceanography award no. OCE 0526332, and the National Oceanic and Atmospheric Administration’s (NOAA) Dr. Nancy Foster or, as has been observed for macroalgae, increased Scholarship Program. The statements, findings, conclusions, and respiration (Finlay and Kendall 2007). Seasonal differ- recommendations are those of the authors and do not necessarily ences in δ13C on the order of 3‰ in particulate organic reflect the views of NSF, NOAA, or the Department of Commerce. 1140 Estuaries and Coasts (2008) 31:1130–1142

References Engineering, Science, and Technology, Inc. 26 Kordahy Street, Roushdie, Alexandria, Arab Republic of Egypt, May 28, 1997. El Atfy, H., H. El Gamaal, and E. Van Mourik. 1991. Discharge rates, Abbas, M.M., L.M. Shakweer, and D.H. Youssef. 2001. Ecological and salinities, and the performance of subsurface collector drains in fisheries management of Edku Lake 1. Hydro-chemical characters Egypt. Irrigation and Drainage Systems 5: 325–338. of Edku Lake. Bulletin of the Institute of Oceanography and doi:10.1007/BF01102830. Fisheries 27: 65–93. El Moghraby, A.I., and A.A. El Rahman. 1984. Food and feeding Abdallah, M.A.M. 2003. The chemical changes in Lake Maryout after habits of Labeo niloticus (Pisces, ) in Jebel Aulia the construction of two wastewater treatment plants. Alexandria: Reservoir, Sudan. Hydrobiologia 110: 327–332. doi:10.1007/ Ph.D. Dissertation, University of Alexandria. BF00025805. Abdel-Moati, M.A.R., and A.A. El-Sammak. 1997. Man-made impact El-Rayis, O. 2005. Impact of man’s activities on a closed fishing-lake, on the geochemistry of the Nile Delta Lakes. A study of metals Lake Maryout in Egypt, as a case study. Mitigation and concentrations in sediments. Water, Air, and Soil Pollution 97: Adaptation Strategies for Global Change 10: 145–157. 413–429. doi:10.1007/s11027-005-7836-9. Abreu, P.C., C.S.B. Costa, C. Bemvenuti, C. Oderbrecht, W. Granéli, El-Sayed, A.F.M. 2006. Tilapia Culture, 1st ed. Oxfordshire: CABI. and A.M. Anesio. 2006. Eutrophication processes and trophic El-Sayed, A.F.M. 2007. Analysis of feeds and fertilizers for interactions in a shallow estuary: preliminary results based on sustainable aquaculture development in Egypt. In Study and stable isotope analysis (δ13C and δ15N). Estuaries and Coasts 29: analysis of feeds and fertilizers for sustainable aquaculture 277–285. development, eds. M.R. Hassan, T.T. Hecht, S.S. De Silva, and Adham, K.G. 2002. Sublethal effects of aquatic pollution in Lake A.G.J. Tacon, 401–422. Rome: FAO, Fisheries Technical Paper. Maryût on the African sharptooth catfish, Clarias gariepinus No. 497. (Burchell, 1822). Journal of Applied Ichthyology 18: 87–94. El-Shenawy, M.A. 1994. Azollla filiculoides, a new effective doi:10.1046/j.1439-0426.2002.00337.x. dinitrogen fixer in Lake Edku, Egypt. Bulletin of the Institute of Al Sayes, A., A. Radwan, and L. Shakweer. 2007. Impact of drainage Oceanography and Fisheries 20: 83–97. water inflow on the environmental conditions and fishery El-Sherif, Z.M., and S.M. Gharib. 2001. Spatial and temporal patterns resources of Lake Borollus. Egyptian Journal of Aquatic of phytoplankton communities in Manzalah Lagoon. Bulletin of Research 33: 312–351. the Institute of Oceanography and Fisheries 27: 217–239. Aly, A.I.M., M.A. Mohamed, and E. Hallaba. 1982. Natural variations Fernandes, C., A. Fontainhas-Fernandes, F. Peixoto, and M.A. of 15N-content of nitrate in ground and surface waters and total Salgado. 2007. Bioaccumulation of heavy metals in Liza saliens nitrogen of soil in the Wadi El-Natrun area in Egypt. In from the Esmoriz–Paramos coastal lagoon, Portugal. Ecotoxicol- Analytical Chemistry Symposia Series Vol. 11, Stable Isotopes, ogy and Environmental Safety 66: 426–431. doi:10.1016/j. Proceedings of the 4th International Conference, Jülich, March ecoenv.2006.02.007. 23–26, 1981, eds. H.L. Schmidt, H. Forstel, and K. Heinzinger, Finlay, J.C., and C. Kendall. 2007. Stable isotope tracing of temporal 475–481. Amsterdam, The Netherlands: Elsevier. and spatial variability in organic matter sources to freshwater Attia, B.B. 2004. Water as a basic human right in Egypt. Global Issue ecosystems. In Stable isotopes in ecology and environmental Papers 11: 36–59. science, eds. R. Michener, and K. Lajtha, 283–333. Malden: Azzurro, E., E. Fanelli, E. Mostarda, M. Catra, and F. Andaloro. 2007. Blackwell. Resource partitioning among early colonizing Siganus luridus Food and Agriculture Organization of the United Nations (FAO). and native herbiverous fish in the Mediterranean: an integrated 2008. FAOSTAT Online Statistical Service. Rome: FAO. http:// study based on gut-content analysis and stable isotope signatures. faostat.fao.org/default.aspx. Accessed 16 April 2008. Journal of the Marine Biological Association of the United Froese, R. and D. Pauly, editors. 2007. FishBase. www.fishbase.org, Kingdom 87: 991–998. doi:10.1017/S0025315407056342. version (10/2007). Accessed 16 April 2008. Bannon, R.O., and C.T. Roman. 2008. Using stable isotopes to Fry, B. 2002. Conservative mixing of stable isotopes across estuarine monitor anthropogenic nitrogen inputs to estuaries. Ecological salinity gradients: a conceptual framework for monitoring Applications 18: 22–30. doi:10.1890/06-2006.1. watershed influences on downstream fisheries production. Estu- Blaber, S.J.M. 1997. Fish and fisheries of tropical estuaries, 1st aries 25: 264–271. edition. London: Chapman and Hall. Fry, B. 2006. Stable Isotope Ecology, 1st edition. New York: Springer. Boynton, W.R., and W.M. Kemp. 2000. Influence of river flow and Fry, B., and Y.C. Allen. 2003. Stable isotopes in zebra mussels as nutrient loads on selected ecosystem processes: a synthesis of bioindicators of river-watershed linkages. River Research and Chesapeake Bay data. In Estuarine Science, a synthetic approach Applications 16: 683–696. doi:10.1002/rra.715. to research and practice, ed. J.E. Hobbie, 269–298. Washington Fry, B., A. Grace, and J.W. McClelland. 2003. Chemical indicators of D.C.: Island. anthropogenic nitrogen loading in four Pacific Estuaries. Pacific Brewer, D.J. 2005. Ancient Egypt: foundations of a civilization, 1st ed. Science 57: 77–101. doi:10.1353/psc.2003.0004. Harlow: Pearson. GAFRD. 2007. Fisheries Statistics Yearbook 2006. Cairo: General Dewidar, K.h., and A. Khedr. 2001. Water quality assessment with Authority for Fish Resources Development (GAFRD). simultaneous Landsat-5 TM at Manzala Lagoon, Egypt. Hydro- Haines, E.B. 1979. Interactions between Georgia salt marshes and biologia 457: 49–58. doi:10.1023/A:1012281416096. coastal waters: a changing paradigm. In Ecological processes in Durborow, R.M., D.M. Crosby, and M.W. Brunson. 1997. Nitrite in coastal and marine systems, 1979. Proceedings of the Sympo- fish ponds. Southern Regional Aquaculture Center (SRAC) sium at Florida State University, April, 1978, ed. R.J. Livingston, Publication No. 462. 4p. http://aquanic.org/publicat/usda_rac/ 35–46. Plenum Press. efs/srac/462fs.pdf/. Accessed 25 June 2008. Hamza, W. 2006. The Nile Estuary. In The handbook of environmental EA Engineering, Science and Technology Inc, 1997. Environmental chemistry vol. 5, part H, ed. P.J. Wangersky, 149–173. Heidel- Technical Report 8 Chemical and Biological Characterization of berg: Springer. Lake Maryout, Final Report. Alexandria Wastewater Project Howarth, R.W., G. Billen, D. Swaney, A. Townsend, N. Jaworski, K. Phase II. USAID Project No. 263–0100. Prepared for Metcalf & Lajtha, J.A. Downing, R. Elmgren, N. Caraco, T. Jordan, F. Eddy International, Roushdie, Alexandria. Prepared by EA Berendse, J. Freney, V. Kudeyarov, P. Murdoch, and Z. Zhao- Estuaries and Coasts (2008) 31:1130–1142 1141

Liang. 1996. Regional nitrogen budgets and riverine N & P Oczkowski, A., and S. Nixon. 2008. Increasing nutrient concentra- fluxes for the drainages to the North Atlantic Ocean: natural and tions and the rise and fall of a coastal fishery; a review of data human influences. Biogeochemistry 35: 75–139. doi:10.1007/ from the Nile Delta, Egypt. Estuarine, Coastal, and Shelf Science BF02179825. 77: 309–319. Iverson, R.L. 1990. Control of marine fish production. Limnology and Oczkowski, A., S. Nixon, K. Henry, P. DiMilla, M. Pilson, S. Granger, Oceanography 35: 1593–1604. B. Buckley, C. Thornber, R. McKinney, and J. Chaves. 2008. Jennings, S., O. Reñones, B. Morales-Nin, N. Polunin, J. Moranta, Distribution and trophic importance of anthropogenic nitrogen in and J. Coll. 1997. Spatial variation in the 15N and 13C stable Narragansett Bay: an assessment using stable isotopes. Estuaries isotope composition of plants, invertebrates and fishes on and Coasts 31: 53–69. Mediterranean reefs: implications for the study of trophic Okbah, M.A. 2005. Nitrogen and phosphorous species of Lake pathways. Marine Ecology Progress Series 146: 109–116. Burullus water (Egypt). Egyptian Journal of Aquatic Research doi:10.3354/meps146109. 31: 186–199. JMP Release 6.0.0. 2005. JMP User Guide, Release 6. Cary: SAS. Okbah, M.A., and S. El-Gohary. 2002. Physical and chemical Jordan, M.J., K.J. Knadelhoffer, and B. Fry. 1997. Nitrogen cycling in characteristics of Lake Edku water, Egypt. Mediterranean forest and grass ecosystems irrigated with 15N-enriched waste- Marine Science 3/2: 27–39. water. Ecological Applications 7: 864–881. Okbah, M.A., and N.R. Hussein. 2006. Impact of environmental Khalil, M.T. 1998. Prediction of fish yield and potential productivity conditions on the phytoplankton structure in Mediterranean Sea from limnological data in Lake Borollus, Egypt. International Lagoon, Lake Burullus, Egypt. Water, Air, and Soil Pollution Journal of Salt Lake Research 6: 323–330. 172: 129–150. doi:10.1007/s11270-005-9066-x. Lehmann, M.F., P. Reichert, S.M. Bernasconi, A. Barbieri, and J.A. Pantoja, S., D.J. Repeta, J.P. Sachs, and D.M. Sigman. 2002. Stable McKenzie. 2003. Modelling nitrogen and oxygen isotope isotope constraints on the nitrogen cycle of the Mediterranean fractionation during denitrification in a lacustrine redox-transition Sea water column. Deep-Sea Research I 49: 1609–1621. zone. Geochimica et Cosmochimica Acta 67: 2529–2542. doi:10.1016/S0967-0637(02)00066-3. doi:10.1016/S0016-7037(03)00085-1. Parker, P.L. 1967. Chemical parameters. In Pollution and Marine Mariotti, A. 1983. Atmospheric nitrogen is a reliable standard for Ecology, eds. T.A. Olsen, and F.J. Burgess, 317–321. New York: natural 15N abundance measurements. Nature 303: 685–687. Interscience. doi:10.1038/303685a0. Radwan, A.-A. 2005. Some factors affecting the primary production McClelland, J.W., I. Valiela, and R.H. Michener. 1997. Nitrogen- of phytoplankton in Lake Burullus. Egyptian Journal of Aquatic stable isotope signatures in estuarine food webs: a record of Research 31: 72–88. increasing urbanization in coastal watersheds. Limnology and Rich, L.G. 2003. Aerated Lagoon Technology. Technical Note Oceanography 42: 930–937. Number 4. Lagoon Systems in Maine. Available at http://www. McIlvin, R.M., and M.A. Altabet. 2005. Chemical conversion of lagoonsonline.com/technote4.htm, accessed 13 May 2008. nitrate to nitrite to nitrous oxide for nitrogen and oxygen isotopic Richards, A. 1982. Egypt’s Agricultural Development 1800–1980, 1st analysis in freshwater and seawater. Analytical Chemistry 77: edition. Boulder: Westview. 5589–5595. doi:10.1021/ac050528s. Roest, C.W.J. 1999. Regional water distribution in the Nile Delta of Munson, S.A., and A.E. Carey. 2004. Organic matter sources and Egypt. Proceedings of the Wageningen Water Workshop, June transport in an agriculturally dominated temperate watershed. 1999, ed. A. Schrevel, 61–81. available online at: http://www2. Applied Geochemistry 19: 1111–1121. doi:10.1016/j.apgeo- alterra.wur.nl/Internet/webdocs/ilri-publicaties/special_reports/ chem.2004.01.010. Srep11/Srep11-h4.pdf. Accessed 28 May 2008. National Water Resources Plan 2017. 2005. Water for the Future. Arab Rogers, K.M. 2003. Stable carbon and nitrogen isotope signatures Republic of Egypt, Ministry of Water Resources and Irrigation. indicate recovery of marine biota from sewage pollution at Moa http://www.wldelft.nl/cons/area/rbm/wrp/index.html. Accessed Point, New Zealand. Marine Pollution Bulletin 46: 821–827. 16 April 2008. doi:10.1016/S0025-326X(03)00097-3. Nixon, S.W. 1988. Physical energy inputs and the comparative Samir, A.M. 2000. The response of benthic foraminifera and ostracods ecology of lake and marine ecosystems. Limnology and Ocean- to various pollution sources: a study from two lagoons in Egypt. ography 33: 1005–1025. Journal of Foraminiferal Research 30: 83–98. doi:10.2113/ Nixon, S.W. 1992. Quantifying the relationship between nitrogen 0300083. input and the productivity of marine ecosystems. In Proceedings Samman, A.A. 1974. Primary production of Lake Edku. Bulletin of of Advanced Marine Technology Conference, vol 5, eds. M. the Institute of Oceanography and Fisheries 4: 260–317. Takahashi, K. Nakata, and T.R. Parsons, 57–83. Tokyo, Japan. Savage, C. 2005. Tracing the influence of sewage nitrogen in a coastal Nixon, S.W. 2003. Replacing the Nile: Are anthropogenic nutrients ecosystem using stable nitrogen isotopes. Ambio 34: 145–150. providing the fertility once brought to the Mediterranean by a doi:10.1639/0044-7447(2005)034[0145:TTIOSN]2.0.CO;2. great river? Ambio 32: 30–39. doi:10.1639/0044-7447(2003)032 Savage, C., and R. Elmgren. 2004. Macroalgal (Fucus vesiculosus) [0030:RTNAAN]2.0.CO;2. δ15N values trace decrease in sewage influence. Ecological Nixon, S.W., J.W. Ammerman, L.P. Atkinson, V.M. Berounsky, G. Applications 14: 517–526. doi:10.1890/02-5396. Billen, W.C. Boicourt, W.R. Boynton, T.M. Church, D.M. Schlacher, T.A., B. Liddel, T.F. Gaston, and M. Schlacher-Hoenlinger. Ditoro, R. Elmgren, J.H. Garber, A.E. Giblin, R.A. Jahnke, N.J. 2005. Fish track wastewater pollution to estuaries. Oecologia P. Owens, M.E.Q. Pilson, and S.P. Seitzinger. 1996. The fate of 144: 570–584. doi:10.1007/s00442-005-0041-4. nitrogen and phosphorous at the land-sea margin of the North Seitzinger, S., J.A. Harrison, J.K. Bohlke, A.F. Bouwman, R. Atlantic Ocean. Biogeochemistry 35: 141–180. doi:10.1007/ Lowrance, B. Peterson, C. Tobias, and G. Van Drecht. 2006. BF02179826. Denitrification across landscapes and waterscapes: a synthesis. Nixon, S.W., B.A. Buckley, S.L. Granger, M. Entsua-Mensah, O. Ecological Applications 16: 2064–2090. doi:10.1890/1051-0761 Ansa-Asare, M.J. White, and R.A. McKinney. 2007. Anthropo- (2006)016[2064:DALAWA]2.0.CO;2. genic enrichment and nutrients in some tropical lagoons of Shakweer, L.M. 2005. Ecological and fisheries development of Lake Ghana, West Africa. Ecological Applications 17: S144–S164. Manzalah (Egypt) 1. Hydrography and chemistry of Lake doi:10.1890/05-0684.1. Manzalah. Egyptian Journal of Aquatic Research 31: 251–269. 1142 Estuaries and Coasts (2008) 31:1130–1142

Shakweer, L.M. 2006. Impacts of drainage water discharge on the Stanley, D.J. 1996. Nile delta: extreme case of sediment entrapment water chemistry of Lake Edku. Egyptian Journal of Aquatic on a delta plain and consequent coastal land loss. Marine Research 32: 264–282. Geology 129: 89–195. doi:10.1016/0025-3227(96)83344-5. Shakweer, L.M., and M.M. Abbas. 2005. Effect of ecological and Toews, D.R., and M.M. Ishak. 1984. Fishery transformation on Lake biological factors on the uptake and concentration of trace Manzala, a brackish Egyptian delta lake in response to elements by aquatic organisms at Edku Lake. Egyptian Journal anthropological and environmental factors during the period of Aquatic Research 31: 271–287. 1920–1980. General Fisheries Council for the Mediterranean Sheats, N. 2000. The use of stable isotopes to define the extent of Studies Review 64: 347–402. incorporation of sewage nitrogen into aquatic food webs and Vizzini, S., and A. Mazzola. 2006. The effects of anthropogenic to discern differences in habitat suitability within a single organic matter inputs on stable carbon and nitrogen isotopes in estuary. Ph.D. Dissertation, Harvard University, Cambridge, organisms from different trophic levels in a southern Mediterra- Massachusetts. nean coastal area. Science of the Total Environment 368: 723– Sigman, D.M., M.A. Altabet, R. Michener, D.C. McCorkle, B. 731. doi:10.1016/j.scitotenv.2006.02.001. Fry, and R.M. Holmes. 1997. Natural abundance-level Vizzini, S., G. Sarà, R.H. Michener, and A. Mazzola. 2002. The role measurement of the nitrogen isotopic composition of oceanic and contribution of the seagrass Posidonia oceanic (L.) Delile nitrate: an adaptation of the ammonia diffusion method. organic matter for secondary consumers as revealed by carbon Marine Chemistry 57: 227–242. doi:10.1016/S0304-4203(97) and nitrogen stable isotope analysis. Acta Oecologia 23: 277– 00009-1. 285. doi:10.1016/S1146-609X(02)01156-6. Skold, M.D., S.A.A. El Shinnawi, and M.L. Nasr. 1984. Irrigation Vizzini, S., B. Savona, T. Do Chi, and A. Mazzola. 2005. Spatial water distribution along branch canals in Egypt: economic variability of stable carbon and nitrogen isotope ratios in a effects. Economic development and cultural change 32: 547– Mediterranean coastal lagoon. Hydrobiologia 550: 73–82. 567. doi:10.1086/451405. doi:10.1007/s10750-005-4364-2.