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African Journal of Aquatic Science
ISSN: 1608-5914 (Print) 1727-9364 (Online) Journal homepage: http://www.tandfonline.com/loi/taas20
Harmful cyanobacteria and their cyanotoxins in Egyptian fresh waters – state of knowledge and research needs
ZA Mohamed
To cite this article: ZA Mohamed (2016) Harmful cyanobacteria and their cyanotoxins in Egyptian fresh waters – state of knowledge and research needs, African Journal of Aquatic Science, 41:4, 361-368, DOI: 10.2989/16085914.2016.1219313
To link to this article: https://doi.org/10.2989/16085914.2016.1219313
Published online: 07 Nov 2016.
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ISSN 1608-5914 EISSN 1727-9364 http://dx.doi.org/10.2989/16085914.2016.1219313
African Journal of Aquatic Science is co-published by NISC (Pty) Ltd and Taylor & Francis Cyanobacterial blooms are one of the major consequences
of eutrophication resulting from the discharge of urban, industrial and agricultural waste into water sources worldwide (Heisler et al. 2008). Cyanobacterial blooms are also favoured by high temperatures (>25 °C) (Merel et al.
2013). Consequently, climate change, particularly global warming, is creating conditions that could favour the growth of harmful cyanobacterial blooms (cyano-HABs) (Paerl and Paul 2012). Risks of cyanobacterial blooms may be signifi- cant when they are found in drinking and recreational water sources (de la Cruz et al. 2013), because most species produce a wide variety of toxins, including hepatotoxins, neurotoxins and dermatotoxins (Codd et al. 2005). Most of these toxins, e.g. microcystins (MCs) are remarkably stable and difficult to remove from drinking water by conventional treatment methods (Dietrich and Hoeger 2005). In addition to their human health threat, cyanotoxins exert acute and chronic lethal and sublethal effects on terrestrial and aquatic plants and animals (Kinnear 2010).
Egypt is located in a dry climatic zone and comprises hyper-arid, arid and semi-arid deserts. Scarce rainfall (yearly average of 40 mm) occurs in most of the south, with a higher rainfall (yearly average of 200 mm) occurring along the area bordering the Mediterranean (Yates and Strzepek 1998). The freshwater water resources in Egypt are limited to the Nile River and its vast network of canals
and groundwater in the delta, the eastern and western deserts and the Sinai (Allam and Allam 2007). With the steady increase in population and the continuous expansion of urbanised areas, pollution has also increased. The Nile River and Egypt’s freshwater lakes are exposed to several sources of pollution, including industrial, municipal and agricultural waste (El-Sheekh 2009). This pollution usually increases nutrient concentrations (particularly nitrogen and phosphorus), leading to the formation of harmful cyanobac- terial blooms (Donohue et al. 2008). Consequently, future availability of freshwater water could be constrained because of poor water quality, thus limiting its use for drinking, recreation and irrigation purposes. Therefore, it is critically important that water sources should be monitored and managed for the presence of harmful cyanobacterial blooms and their cyanotoxins. This extensive review aims to provide current state of knowledge about cyanobacterial blooms and their cyanotoxins in Egyptian fresh waters and identify research gaps and needs.
Cyanobacterial blooms and cyanotoxins in the Nile River Since the early part of the last century, there have been many investigations studying the phytoplankton community structure and abundance in the Nile River stream (Talling et al. 2009; El-Otify and Iskaros 2015). Data in this review
Review Paper Harmful cyanobacteria and their cyanotoxins in Egyptian fresh waters – state of knowledge and research needs
ZA Mohamed
Department of Botany and Microbiology, Faculty of Science, Sohag University, Sohag, Egypt e-mail: [email protected]
Cyanobacterial blooms have increased in freshwater ecosystems worldwide in the last century, mostly resulting from eutrophication and climate change. These blooms represent serious threats to environmental and human health because of the production of harmful metabolites, called cyanotoxins. Like many countries, Egypt has been plagued with cyanobacterial blooms in most water sources, including the Nile River, irrigation canals, lakes and fishponds. However, the data about cyanotoxins produced in these blooms are limited. Only two types of cyanotoxins, microcystins and cylindrospermopsin, have been identified and characterised, mainly from Microcystis and Cylindrospermopsis blooms. The data revealed the presence of microcystins in raw and treated drinking waters at concentrations (0.05–3.8 µg l−1), exceeding the WHO limit (1 µg l−1) in some drinking water treatment plants. In addition, Nile tilapia Oreochromis niloticus caught from ponds containing heavy cyanobacterial blooms have accumulated considerable amounts of cyanotoxins in their edible tissues. The data presented here could be the catalyst for the establishment of a monitoring and management programme for harmful cyanobacteria and their cyanotoxins in Egyptian fresh waters. This review also elucidates the important research gaps and possible avenues for future research on cyanobacterial blooms and cyanotoxins in Egypt.
Keywords: eutrophication, harmful blooms, hepatotoxins, neurotoxins, water quality
Introduction
Published online 07 Nov 2016
Mohamed 362
were collated from available publications and from disser- tations in local libraries between 1909 and 2016. In spite of the fact that algal bloom development is limited in rivers (Soares et al. 2007; Karadžić et al. 2013), few studies reported the presence of cyanobacterial blooms in the Nile River embayments (khors) where residence time and low flow velocity allow sufficient time for their growth and reproduction in the presence of nutrient enrichment, as suggested by Soares et al. (2007) and Piirsoo et al. (2008).
Microcystis aeruginosa is a common bloom-forming species found in the main Nile River. Microcystis blooms were reported year-round in the upper Nile region (Mohamed and Carmichael 2000; Ali 2004) (Figure 1) and were found to produce microcystin toxins at concentrations up to 250 µg l−1 (Tables 1 and 2). The main microcystin variant produced by all such blooms was MC-LR, the most toxic microcystin in this family of toxins (Ali 2004).
Microcystis blooms were also recorded in the Nile Delta (Hamed 2005; Gomaa et al. 2014; Mohamed et al. 2015;
Figure 1), but toxin production in these blooms was rarely documented. Amer et al. (2009) demonstrated the diversity of hepatotoxic cyanobacteria in water samples from the Nile Delta using denaturing gradient gel electrophoresis (DGGE) fingerprinting and real-time PCR. However, the authors did not report the toxin quantities produced by these species, though they described that the hepato- toxin concentrations in the water samples were below the detection limit of ELISA (0.1 µg l−1). Very recently, Mohamed et al. (2015) demonstrated that a Microcystis bloom found around the intake of drinking water treatment plants in Damietta (Figure 1) can produce two microcystin variants, one containing the amino acids leucine (L) and arginine (R) (MC-LR) and the other containing two arginine (R) amino acids (MC-RR) with total concentrations reaching 341 µg l−1 (Table 2). In addition to Microcystis blooms, other cyanobac- terial blooms were also detected in the Nile River. For instance, Oscillatoria tenuis and Oscillatoria limnetica formed harmful blooms in the Nile near the intakes of drinking water treatment plants (DWTPs) at Sohag city, containing MCs at concentrations of 300 and 877 µg l−1, respectively (Brittain et al. 2000; Mohamed 2016). Blooms of Oscillatoria brevis and Oscillatoria princeps were also recorded in the Nile Rosetta branch of Nile Delta during winter (December–
February) (Gomaa et al. 2014; Figure 1), but toxin produc- tion in these blooms has not been documented. Besides blooms of planktonic species, cyanobacteria were found to form benthic mats on the Nile River banks in Sohag province (Figure 1). These mats contained toxic species belonging to the families Nostocaceae and Oscillatoriaceae (Mohamed et al. 2006; Table 1) and produced high concentrations of MCs (1 600–4 100 µg g−1) with different toxin profiles, MC-LR and MC-YR, the latter containing the amino acids tyrosine (Y) and arginine (R). In addition to the production of hepato- toxic MCs, these benthic cyanobacteria exhibited neurotox- icity in mice, displaying symptoms similar to those caused by saxitoxins or neosaxitoxins (Mohamed et al. 2006; Table 1).
Cyanobacterial blooms and cyanotoxins in irrigation canals Irrigation canals similarly exhibited the presence of cyano- bacterial blooms. Planktothrix agardhii (formerly Oscillatoria
agardhii) dominated phytoplankton populations and formed blooms in irrigation canals in Upper Egypt, containing the green alga Spirogyra during the period May–September 2000, whereas it had a moderate/rare occurrence in the canals not containing Spirogyra (Table 2). This species was found to produce MCs at concentrations of 145 µg g−1 (Mohamed 2002). In the Suez freshwater canal, the sole drinking water supply for Suez City, blooms of M. aerugi- nosa, O. formosa and O. princeps were observed during the period of December 2003 to February 2004 (El-Manawy and Amin 2004). The blooms were associated with increased nutrients (particularly, NH4, NO3 and PO4) and suitable temperature (17–23 °C). Occurrence of cyanobacterial blooms during winter (17–23 °C) in Egyptian fresh waters nowadays might be resulting from climatic change and global warming, compared to lower temperatures (13–18 °C) recorded in the past (Saad and Abbas 1985; Gharib 2006).
These results therefore support earlier suggestions that global warming favours regional cyanobacterial blooms expansion and lengthens the periods of bloom persis- tence (i.e. year-round) in eutrophic waterbodies (Paerl and Huisman 2008; Paerl and Paul 2012; Gkelis et al. 2014).
In addition to planktonic cyanobacteria, irrigation canals in Egypt are usually covered with benthic mats of cyanobac- teria, particularly when the water levels decrease because of water management regimes. This may reflect altered mixing and sedimentation within the irrigation canals. Irrigation
Cairo
Sohag
Luxor
Aswan
RED SEA
0 200 400 km
EGYPT
Egypt MEDITERRANEAN SEA
26° N 28° N
24° N 30° N 32° N
30° E 32° E 34° E 36° E
AFRICA
Nile
Nile
Nile NasserLake QarunLake
Wadi El-Rayah Lakes
Port Said Alexandria
Fayum Damietta Rosetta
SuezCity
Figure 1: Map showing locations of cyanobacterial blooms (white stars) in Egyptian waters from 1909 to 2016
Water source Location Bloom/mat-forming
species Toxin
produced Amount of
toxin (µg g−1) Reference Nile River Middle Nile
Nile Delta, Damietta Nile Delta, Rosetta
Microcystis aeruginosa MCs MCs ND
250 341 ND
Mohamed and Carmichael 2000;
Ali 2004 Amer et al. 2009;
Mohamed et al. 2015 Gomaa et al. 2014 Middle Nile – bloom Oscillatoria tenuis MCs 300 Brittain et al. 2000 Middle Nile – benthic mats Anabaena subcylindrica MCs 3 000 Mohamed et al. 2006
Anabaena variables MCs 1 600 Mohamed et al. 2006 Nostoc spongiaeforme MCs 4 100 Mohamed et al. 2006
Oscillatoria brevis ND ND Gomaa et al. 2014
Oscillatoria princeps ND ND Gomaa et al. 2014
Phormidium corium MCs 2 100 Mohamed et al. 2006
Calothrix parietina Saxitoxin
symptoms LD50 =
560 mg kg−1 Mohamed et al. 2006 Intakes of treatment plants Oscillatoria limnetica MCs 877 Mohamed 2016 Irrigation canals Upper Egypt – blooms Planktothrix agardhii MCs 145 Mohamed 2001
Upper Egypt – mats Anabaena variables MCs 1 900 Mohamed et al. 2006 Nostoc spongiaeforme MCs 4 700 Mohamed et al. 2006 Plectonema boryanum MCs 2 650 Mohamed et al. 2006 Phormidium tenue Saxitoxin
symptoms LD50 =
270 mg kg−1 Mohamed et al. 2006 Delta region – blooms Microcystis aeruginosa ND ND El-Manawy and Amin 2004
Oscillatoria formosa ND ND El-Manawy and Amin 2004
Oscillatoria princeps ND ND El-Manawy and Amin 2004
Fishponds Upper Egypt
Microcystis aeruginosa MCs 4 500 Mohamed 1998; Mohamed et al. 2003
Cylindrospermopsis
raciborskii CYN LD50 =
450 mg kg−1 Mohamed et al. 2007 Raphidiopsis
mediterranea Anatoxin-a
symptoms LD50 =
360 mg kg−1 Mohamed et al. 2007
El-Fayum Anabaenopsis circularis ND ND Konsowa 2007
Lakes Lake Nasser, southern part Microcystis aeruginosa ND ND Mohamed and Loriya 2000; El-Otify et al. 2003; Abd El-Monem 2008; Hussian et al. 2015 Anabaenopsis
cunningtonii ND ND El-Otify et al. 2003; Gharib and
Abdel-Halim 2006 Planktolyngbya limnetica ND ND Hussian et al. 2015
Wadi El-Rayian, upper lake Microcystis aeruginosa ND ND Konsowa and Abd Ellah 2002;
Abd El-Karim 2004; Abd El-Fatah 2010; Khalifa and Abd El-Hady 2010
Microcystis flos-aquae ND ND Konsowa and Abd Ellah 2002;
Abd El- Karim 2004; Abd El-Fatah 2010; Khalifa and Abd El-Hady 2010 Lake Qarun, eastern part Microcystis aeruginosa ND ND Abd El-Fatah 2010
Microcystis flos-aquae ND ND Abdel-Malek and Ishak 1980;
Fathi and Flower 2005; Abd El-Fatah 2010
Table 1: Harmful cyanobacteria and their cyanotoxins reported in Egyptian fresh waters from 1909 to 2016. MC = microcystin, CYN = cylindrospermopsin, ND = cyanotoxins not determined, LD50 determined by administering cyanobacterial extracts intraperitoneally to albino mice
canal mats had similar species composition with Nile River mats (Table 1) and MC-producing species contained the same toxin profile (MC-LR and MC-YR). However, irriga- tion canal species were found to produce greater quanti- ties of toxins (1 900–4 700 µg g−1) than those of the Nile River (Mohamed et al. 2006; Table 1). Irrigation canal mats also contained potentially neurotoxic species, such as
Phormidium tenue, which resulted in saxitoxin symptoms in exposed mice (Mohamed et al. 2006).
Cyanobacterial blooms and cyanotoxins in lakes
Over the past three decades, blooms of M. aeruginosa have been reported in Lake Nasser (Figure 1), particularly
Mohamed 364
the southern part (Bishai et al. 2000; Mohamed and Loriya 2000; El-Otify et al. 2003; Gharib and Abdel-Halim 2006;
Abd El-Monem 2008; Hussian et al. 2015). Microcystis blooms tend to occur year-round in this lake (Mohamed and Loriya 2000), because suitable growth conditions of high temperature and increased nutrient concentrations are found. Although Lake Nasser is considered mesotrophic (Mageed and Heikal 2006), the southern part is eutrophic (Ndebele-Murisa et al. 2010). Other cyanobacterial blooms of Anabaenopsis cunningtonii (El-Otify 2003) and Planktolyngbya limnetica (Hussian et al. 2015) were also detected in Lake Nasser during summer on a yearly basis.
Nevertheless, cyanotoxin production by these blooms has not been documented yet. Wadi El-Raiyan Lakes, Fayum Governorate (Figure 1), have exhibited extensive blooms of M. aeruginosa and M. flos-aquae during the winter season (temperature range = 17–23 °C) in the upper lake, correlating with low salinity (1.5 g l−1) and high nutrient concentrations compared to high salinity and low nutrient concentrations in the lower lake (Konsowa and Abd Ellah 2002; Abd El-Fatah 2010). These Microcystis blooms occur yearly from December to May, followed by Planktolyngbya limnetica blooms during the summer months; causing adverse toxic effects on economically valued fishes in the lake (Nasr et al. 2012). However, the toxicity of these blooms has not been investigated yet. Lake Qarun (northern Fayum Depression; Figure 1) has experienced cyanobac- terial blooms since it was a freshwater lake (West 1909), being connected with the Nile River. Despite becoming slightly saline, Lake Qarun still exhibits cyanobacterial blooms particularly in the eastern part of the lake, because of low salinity (10–14 g l−1) and high nutrient concentrations resulting from large amounts of freshwater discharged to the east of the lake compared to high salinity (38–42 g l−1) in the middle and western parts (El-Shabrawy and Dumont 2009).
The most common water-bloom-forming species prevalent in Lake Qarun are Microcystis aeruginosa and M. flos-aquae.
These species usually bloom year-round in the eastern part of the lake (Fathi and Flower 2005; Abd El-Fatah 2010).
Despite the potential risks of these cyanobacterial blooms to the fisheries and wild life in the lake, no data are available so far for toxins contained in these blooms.
Cyanobacterial blooms and cyanotoxins in fishponds Aquaculture in Egypt, including earthen ponds, concrete ponds and floating cages, has witnessed many pollution problems and fish kills. Nile River water is the main source of water for these fish farms. One of the main problems is eutrophication caused by nutrient enrich- ment resulting from the addition of fertilisers and supple- mentary feed to the pond water to raise fish. This leads to reduction of oxygen, outgassing of hydrogen sulphide and phytoplankton blooms (Boyd 2006). The presence of harmful blooms, e.g. cyanobacterial blooms in fishponds, is of particular concern for environmental and human health, because they can produce potent toxins that cause fish mortality and accumulate in fish muscles with potential transfers to humans upon consumption (Mohamed et al.
2003). Many phytoplankton studies have reported the occurrence of cyanobacterial blooms in both freshwater and saline fishponds in Egypt (Mohamed et al. 1986, 2003; Konsowa 2007; Mohamed 2007). However, only a few studies have investigated the toxin production in these blooms. Mohamed et al. (2003) found that M. aerugi- nosa blooms in El-Dowyrat fishpond (Sohag Governorate, Figure 1) produce MCs at concentrations of 1 120 µg g−1, with a profile consisting of MC-RR, MC-YR and MC-WR.
These blooms were observed year-round on the surface of this pond. El-Dowyrat fishpond also exhibited extensive blooms of Cylindrospermopsis raciborskii and Raphidiopsis mediterranea during the warm months of 2002 and 2003 (Mohamed 2007; Tables 1 and 2) and these blooms still appear each year in this pond from June to August (ZAM pers. obs.). These blooms are exclusively limited to high temperatures (>25 °C) that are required for the germina- tion of Cylindrospermopsis and Raphidiopsis akinetes (Mohamed 2007). The crude extract of C. raciborskii strains isolated from this bloom did not show any signs of neurotoxicity, but exhibited hepatotoxic symptoms in the mouse bioassay, as reported for other cylindrospermopsin- producing Cylindrospermopsis (Mohamed 2007). Recently, our team quantified cylindrospermopsin toxin levels up to 2.7 µg l−1 in Cylindrospermopsis blooms (i.e. within cells) from other fishponds located in the Sohag Governorate Water source Location Toxin Particulate
toxins (µg l−1) Extracellular
toxins (µg l−1) Treated
water (µg l−1) Toxin in
animal tissues Reference Nile River, upper
Nile Microcystis bloom Benthic mats Oscillatoria bloom
MCs
MCsMCs
250
1 600–4 100 0.7–1.4
0.4–0.8
0.05–0.8ND
0.05–0.1
0.4–3.8ND
ND
NDND
Mohamed and Carmichael 2000;
Ali 2004
Mohamed et al. 2006 Mohamed 2015
Nile Delta Microcystis bloom MCs 341 1.6–4.5 1.1–3.6 ND Mohamed et al. 2015
Irrigation canals Microcystis bloom MCs 890 ND ND 0.1 µg daphnid−1 Mohamed 2001
Oscillatoria bloom MCs 110 ND ND ND Mohamed 2002
Benthic mats MCs 1 600–3 000 ND ND ND Mohamed et al. 2006
Fishponds Microcystis bloom MCs 1 120 ND ND 0.1 µg g−1 tilapia fish Mohamed et al. 2003 Cylindrospermopsis
blooms CYN 0.6–2.7 0.4–2.5 ND ND ZAM unpublished
data
Table 2: Cyanotoxin concentrations in raw and treated water and their accumulation in aquatic food webs in Egypt. MC = microcystin; CYN = cylindrospermopsin; ND = cyanotoxins not determined
(Figure 1) and these blooms were found to excrete high concentrations of dissolved cylindrospermopsin (2.4 µg l−1) into the fishpond water (Ahmed 2016). To our knowledge and based on the review of Rzymski and Poniedziałek (2014), this is the first study to report cylindrospermopsin production by C. raciborskii strains in Africa. In contrast, R. mediterranea extract showed signs of neurotox- icity, similar to those of cyanobacterial extract containing anatoxin-a (Mohamed 2007; Table 1). Other cyanobacterial species were also observed to form water blooms in fishponds, e.g. Anabaenopsis blooms found in a fish farm in El-Fayoum (Konsowa 2007; Figure 1). However, there are currently no available data about toxins produced by these blooms.
Potential health risks associated with cyanotoxins in Egyptian fresh waters
Generally, humans may be exposed to toxic cyanobacteria or their cyanotoxins through the swallowing of water during swimming, drinking unsuitably treated water and consump- tion of contaminated food (fish, vegetable plants and food supplements derived from cyanobacteria) (Drobac et al.
2013). All of these routes of exposure are likely to occur in Egypt, because cyanotoxins were detected in drinking and recreational waters and in edible tissues of fish (Table 2).
The WHO has set provisional guidelines (1 µg l−1) for the consumption of MCs (WHO 1998), which was grossly exceeded in some Egyptian water sources (Mohamed et al. 2003; Table 2). The presence of such high concentra- tions of MCs in drinking and recreational waters poses a risk to humans and to both domesticated and wild animals that consume such water. The occurrence of cyanotoxins in finished drinking water depends on their levels in the source water and the effectiveness of treatment methods for removing cyanobacteria and cyanotoxins in drinking water treatment plants. In Egypt, MCs were detected in the source water of some drinking water treatment plants at concentrations ranging from 0.7 to 341 µg l−1. Because Egypt has adopted the WHO guideline limit of 1 µg l−1 and tolerable daily intake (TDI) of 0.04 µg kg−1 body weight (Kuiper-Goodman et al. 1999), MC concentrations detected in finished water of some DWTPs (1.1–3.8 µg l−1) exceed these thresholds and might pose a risk to human health. On the other hand, finished drinking water of other treatment plants had MC concentrations (0.05–0.4 µg l−1) below the WHO limit but close to the chronic exposure limit (0.1 µg l−1) proposed by Hoeger et al. (2005) and at which possible tumour-promoting activities of MCs occur. This illustrates the importance of proper treatment methods used for removing cyanotoxins from drinking water.
Conventional methods (preoxidation, coagulation, floccu- lation, sedimentation and chlorine disinfection) used in DWTPs in most countries, including Egypt, are not adequate for removing cyanotoxins. They may be effective in removing cyanobacterial cells, but not in intact form, because prechlorination damages the cells leading to the toxin release into the clean water. This explains the drastic increase in the concentrations of extracellular MCs in the flocculant water (3.1–7.1 µg l−1) compared with the source water (1.6–4.5 µg l−1) in some Egyptian DWTPs (Mohamed
et al. 2015; Mohamed 2016; Table 2). Therefore, the use of the prechlorination step at DWTPs should be avoided, because it exacerbates the problem rather than eliminating cyanobacterial cells from the water. On the other hand, the sludge of the clarifiers of Egyptian DWTPs was found to contain high concentrations of MCs ranging from 4.2 to 9.1 µg l−1 (Mohamed et al. 2015). This deliberately contrib- utes to MCs burden in the flocculant water, because the cells contained in the sludge break down rapidly and release their toxins into the clarifier water (Zamyadi et al.
2012).
Therefore, it is advisable to remove sludge from sedimentation basins rapidly to prevent or minimise the release of cyanotoxins from the sludge beds. Because the Nile River raw water could be used for recreation, the presence of MCs may pose a risk to people bathing or recreating in these waters. This risk can be calculated by applying the following the formula of Gkelis et al. (2015) to estimate the amount of water that has to be consumed to reach the tolerable daily intake (TDI; 0.04 µg kg−1 body weight) threshold set by Kuiper-Goodman et al (1999):
Aw = (TDI × BW) ∕ ΣMC
where Aw is the amount of water (litres) that have to be accidentally consumed to reach TDI threshold (0.04 µg kg−1 body weight), BW is a child (10 kg) or adult (60 kg) average body weight (kg) and ΣMC is the total MC concentration (µg l−1) in raw water (calculated from data in Table 2). In the Nile River water in the southern regions of Egypt, accidental ingestion by children and adults of 1.6–10 ml of water during recreation would result in doses exceeding the WHO TDI (0.04 µg kg−1 body weight), whereas ingestion of 1–6 ml of Nile water at the Nile Delta during recreation would yield doses surpassing the WHO TDI threshold.
In addition to their presence in drinking and recreational water, cyanotoxins can accumulate in the tissues of aquatic organisms, including mussels, crayfish and fish used for human consumption when feeding on toxic cyanobacteria and thus pose a health hazard to humans consuming them.
In this respect, tilapia from Egyptian fishponds were found to accumulate MCs in edible tissues at concentrations as high as 102 ng g−1 fresh weight, compared to the total toxin concentration accumulated in different organs (Mohamed et al. 2003; Table 2). Based on the average amount of fish eaten by a person (100 g serving−1), toxin concentra- tions entering the human body amounts to 10 µg serving−1, or approximately five times the recommended daily toxin intake (2 litres day−1 containing 1 µg l−1 MC) from drinking water. Because microcystin toxins are heat stable and not broken down by cooking, fish from these sources may pose a serious health hazard to consumers (Zhang et al. 2010).
In addition to fish, Daphnia were found to accumulate MCs (0.1 µg daphnid−1) in its body during feeding on toxic blooms of M. aeruginosa in Egyptian irrigation canals (Mohamed 2001; Table 2). Therefore, the primary consumers (e.g.
Daphnia) may act as reservoirs and vectors transfer- ring cyanotoxins to animals higher up the trophic chain, including humans (Gutiérrez-Praena et al. 2013). Finally, toxic cyanobacteria and/or their cyanotoxins can migrate
Mohamed 366
from neighbouring water sources by wind and rainfall that settles onto desert crusts (Dubovik 2002; Pringault and Garcia-Pichel 2004).
Therefore, potentially harmful cyanobacteria may contri- bute significantly to the total air particle load (Genitsaris et al. 2011), posing a risk to human when inhaling particles containing cyanotoxins (Metcalf et al. 2012). Furthermore, airborne akinetes and spores of toxic cyanobacteria may invade and germinate in other water sources, particularly domestic storage reservoirs and tanks, forming harmful biofilms on the water surface.
Research gaps and needs
Analysis of the available literature on phytoplankton analysis in the freshwater ecosystems of Egypt has revealed a number of gaps that require additional and collaborative efforts from researchers and authorities. The majority of these studies have described only the seasonal abundance and bloom dynamics of cyanobacterial species, ignoring toxins produced by these blooms. Although a few studies investigated the toxin production in cyanobacterial blooms, they focused only on two types of cyanotoxins: microcystins and cylindrospermopsin.
Further research is consequently needed in order to study the potential production of other cyanotoxins, e.g.
saxitoxins, anatoxins, β-N-methylamino-l-alanine (BMAA), and dermatotoxins (lyngbyatoxins and aplysiatoxins) by cyanobacterial blooms. In addition to known toxins, other cyanobacterial bioactive compounds with currently unknown biological activities should be investigated as well, because they may exert toxic effects stronger than those of cyanotoxins. Because cyanobacterial blooms and cyanotoxins were detected in Egyptian water sources, there is an urgent need for monitoring programmes for cyanobacteria. Indeed, the greater awareness concerning cyanobacterial blooms and their cyanotoxins in Egypt has been at a scientific level, but it has not been reflected at a national governmental level in terms of the development of monitoring programmes and legislation.
In addition, there have been no reported cases of human or animal poisoning as a result of exposure to cyanobacte- rial toxins in Egypt, although the dangers of cyanobac terial toxins associated with blooms are a global issue and are being addressed nationally or regionally (Donohue et al.
2008). This is probably the result of a lack of knowledge of the general public, vets and physicians about cyanotoxins in Egypt. Therefore, misdiagnosis of some cyanotoxin- poisoning cases may have occurred. This reflects the large gap between environmental toxicologists and the medical community in this country. The recognition of the health hazards of cyanotoxins in Egypt is an important factor for the development of risk management strategies.
Therefore, an effective risk management programme for cyanobacteria and cyanotoxins in Egyptian water sources should be undertaken by experts in multiple fields, such as biology, chemistry, toxicology, medicine, public health, water engineering and water suppliers. This manage- ment programme will enable responsible agencies to set guidelines and limits to protect human, animals, plants and water sources from such potent toxins.
Conclusions
This review highlights the need for more work on monitoring and management of cyanobacteria and cyanotoxins in Egyptian water sources. This should be carried out at a national governmental level in order to estimate guideline limits for these cyanotoxins in drinking water sources and fish to protect public health.
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Manuscript received 17 November 2015, revised 20 June 2016, accepted 28 July 2016 Associate Editor: JC Taylor