Hostname: page-component-7b7567c8c-mnklg Total loading time: 0 Render date: 2026-11-12T09:04:50.209Z Has data issue: false hasContentIssue false
  • English
  • Français

Interactions between the intestinal cestode Polyonchobothrium clarias (Pseudophyllidea: Ptychobothriidae) from the African sharptooth catfish Clarias gariepinus and heavy metal pollutants in an aquatic environment in Egypt

Published online by Cambridge University Press:  08 January 2016

R. Abdel-Gaber,
F. Abdel-Ghaffar,
A.-R. Bashtar,
K. Morsy and
R. Saleh
R. Abdel-Gaber*
Affiliation:
Zoology Department, Faculty of Science, Cairo University, Cairo, Egypt
F. Abdel-Ghaffar
Affiliation:
Zoology Department, Faculty of Science, Cairo University, Cairo, Egypt
A.-R. Bashtar
Affiliation:
Zoology Department, Faculty of Science, Cairo University, Cairo, Egypt
K. Morsy
Affiliation:
Zoology Department, Faculty of Science, Cairo University, Cairo, Egypt
R. Saleh
Affiliation:
Zoology Department, Faculty of Science, Cairo University, Cairo, Egypt
*
*E-mail: rewaida@sci.cu.edu.eg
Rights & Permissions [Opens in a new window]

Abstract

In an aquatic environment, there is a profound and inverse relationship between environmental quality and disease status of fish. Parasites are one of the most serious limiting factors in aquaculture. Therefore, the present investigation was carried out during the period of February–December 2014 to determine the parasitic infections in the African sharptooth catfish Clarias gariepinus, relative to the capability of internal parasites to accumulate heavy metals. Up to 100 catfish were examined for gastrointestinal helminths and 38% of fish were found to be infected with the cestode Polyonchobothrium clarias. The morphology of this parasite species, based on light and scanning electron microscopy, revealed that the adult worm was characterized by a rectangular scolex measuring 0.43–0.58 (0.49 ± 0.1) mm long and 0.15–0.21 (0.19 ± 0.1) mm wide, with a flat to slightly raised rostellum armed with a crown with two semicircles each bearing 13–15 hooks, followed by immature, mature and gravid proglottids which were about 29–55 (45), 16–30 (24) and 15–39 (28) in number, respectively. The mature proglottid contained a single set of genitalia in which medullary testes measured 0.09–0.13 (0.11 ± 0.01) mm long and 0.05–0.08 (0.06 ± 0.01) mm wide; a bi-lobed ovary was situated near the posterior margin of the proglottid, extending laterally up to the longitudinal excretory canals; the tubular uterus arose from the ootype up to the anterior margin of the proglottid; and vitelline follicles were cortical. The greater portion of the gravid proglottid was occupied by a uterus filled with unoperculate and embryonated eggs. Chemical analysis confirmed that the concentrations of heavy metals (Zn, Cu, Mn, Cd, Ni and Pb) accumulated in P. clarias were higher than in fish tissues and values recommended by FAO/WHO, with the exception of Zn, which was found to be higher in fish kidneys than in the cestode. This supports the hypothesis that cestodes of fish can be regarded as useful bioindicators when evaluating the environmental pollution of aquatic ecosystems by heavy metals.

Information

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 6 , November 2016, pp. 742 - 752
Copyright
Copyright © Cambridge University Press 2016 

Introduction

The African sharptooth catfish, Clarias gariepinus Burchell, 1822, is generally considered to be one of the most important tropical catfish species for aquaculture in West Africa (Awachie & Ezenwaji, Reference Awachie and Ezenwaji1981; Abdel-Gaber et al., Reference Abdel-Gaber, El Ghary and Morsy2015). This African catfish is widely distributed throughout Africa, inhabiting tropical swamps, lakes and rivers (Olufemi et al., Reference Olufemi, Akinlabi and Agbede1991). With growing interest in the development of aquaculture, there is also an increase in the awareness of the role of parasites as a biological indicator for different forms of pollution in the aquatic environment (Dural et al., Reference Dural, Genc, Sangun and Güner2011). The relationship between pollution and parasitism in aquatic organisms and the potential role of parasites as water quality indicators have received increasing attention during the past two decades (Marcogliese et al., Reference Marcogliese, Brambilla, Gagne and Gendron2005, Reference Marcogliese, King, Salo, Fournier, Brousseau, Spear, Champoux, McLaughlin and Boily2009, Reference Marcogliese, Dautremepuits, Gendron and Fournier2010; Sures, Reference Sures2008; Abdel-Ghaffar et al., Reference Abdel-Ghaffar, Abdel-Gaber, Bashtar, Morsy, Mehlhorn, Al Quraishy and Saleh2014). Several studies have revealed rich parasitic fauna in freshwater fish, ranging from ecto- to endoparasites, which affect fish health, growth and survival (Oniye et al., Reference Oniye, Adebote and Ayanda2004). The helminth fauna of African teleosts has been studied since the middle of the 19th century, when Leydig (Reference Leydig1853) and Wedl (Reference Wedl1861) described the first tapeworms from bichirs and clariid fish, respectively. According to Paperna (Reference Paperna1996), cestodes occur almost exclusively in siluriform fish, most commonly in Clariidae and Polypteridae. Polyonchobothrium clarias was of much interest because it was among the important cestodes that might have a tendency to interfere with the nutritive element of their hosts, as most of these worms prefer to localize in gastric and intestinal regions where the maximal intestinal absorption is performed (Sures et al., Reference Sures, Scheef, Klar, Kloas and Taraschewski2002; Mohammed, Reference Mohammed2012; Abdel-Gaber et al., Reference Abdel-Gaber, El Ghary and Morsy2015). This cestode species was first described by Woodland (Reference Woodland1925) from the Sudanese Clarias anguillaris under the name Clastobothirium clarias. Janicki (Reference Janicki and Jägerskiöld1926) described the parasite from Egyptian Clarias anguillaris in more detail, proposing the occurrence of short and long forms, so both Polyonchobothrium cylindericum minor and Polyonchobothrium cylindericum were assigned to Clastobothirium clarias Woodland (Reference Woodland1925). Tadros (Reference Tadros1966) re-described P. clarias and synonymized it with P. cylindericum minor (Janicki Reference Janicki and Jägerskiöld1926). Imam (Reference Imam1971), Negm-El Din (Reference Negm-El Din1987), Hassan (Reference Hassan1992) and Ramadan (Reference Ramadan1994) re-described the parasite as P. clarias.

Therefore the aim of the present investigation was to evaluate the effect of P. clarias within the African catfish as a bioindicator for metal accumulation in Lake Manzala, Egypt. In addition, morphological and morphometric characteristics for the recovered species were carried out using light and scanning electron microscopy, to determine its exact taxonomic position within the family Ptychobothriidae.

Materials and methods

Collection and examination of fish and cestodes

Lake Manzala is the largest lake in the north-east quadrant of the Nile Delta, Egypt (Bahnasawy et al., Reference Bahnasawy, Khidr and Dheina2011) (fig. 1). It extends between 31°45′–32°22′E and 31°00′–31°30′N. It is bordered by the Mediterranean Sea at the north, the Suez Canal at the east, Damietta province in the north-west, and Dakahlia province in the south-west. A total number of 100 African catfish C. gariepinus (Family Clariidae) were caught, using gill nets, during the period of February–December 2014, i.e. 25 fish per season. Fish were kept in glass aquaria and supplied with chlorine-free tap water with continuous aeration and filtration, according to Innes (Reference Innes1966), to be transferred to the Laboratory of Parasitology Research at the Zoology Department, Faculty of Science, Cairo University, Egypt. Fish samples were identified based on the external features, as described by Idodo-Umeh (Reference Idodo-Umeh2003). Fish were sacrificed by severing the spinal cord behind the head and were then dissected by making an insertion from the anus towards the head. The intestine of each fish was removed, placed in 0.6% physiological saline solution in a Petri dish and opened up to observe and count any emerging helminths. The prevalence and mean intensity of infection were evaluated according to Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997). Cestodes were relaxed in saline solution, fixed in hot alcohol–formalin–acetic acid (AFA) solution, preserved in 70% alcohol and then stained with Semichon's acetocarmine stain, according to Woodland (Reference Woodland2006). Cestodes were recovered and identified according to the identification key of Yamaguti (Reference Yamaguti1961). For scanning electron microscopy, specimens were fixed in 3% glutaraldehyde (pH 7.2) for 4 h, then washed in sodium cacodylate buffer and dehydrated in a graded series of ethanol. After passing through an ascending series of Genosolv-D (HIO, Morristown, USA) they were processed in a critical point drier ‘Bomer-900’ with Freon 13, and sputter-coated with gold–palladium in a Technics Hummer V, then examined and photographed under an Etec Auto scan (QMSI, San Diego, California, USA) at 20 kV. All drawings were made with the aid of a camera lucida. Measurements were taken in millimetres, as a range followed by mean ±  SD in parentheses, unless otherwise stated.

Fig. 1

Geographical location of Lake Manzala, Dakahlia province, Egypt.

Chemical and data analyses

Fish and parasite tissues were analysed to detect heavy metals, according to the procedure described by UNEP/FAO/IOC/IAEA (1984). Samples were digested with concentrated nitric acid and perchloric acid (2:1 v/v) at 60°C for 3 days. After the complete digestion, samples were diluted with bi-distilled water and then analysed for trace elements in an inductively coupled plasma mass spectrometer (Varian Model-Liberty Series II, Analytical West, Inc., Corona, California, USA) using a flame and graphite furnace technique. Values of all monitored heavy metals are presented in μg/g wet-weight, comparing with values detected by FAO/WHO (2004). The absorption wavelengths and detection limits for the heavy metals by using an Elbert mount diffraction grating monochromator (Horiba Scientific, New Jersey, USA) were, respectively, 217.0 nm and 0.001 ppm for Pb, 228.8 nm and 0.002 ppm for Cd, 279.5 nm and 0.01 ppm for Mn, 213.9 nm and 0.001 ppm for Zn, 324.7 nm and 0.02 ppm for Cu, and 232.0 nm and 0.01 ppm for Ni. In addition, the bioaccumulation factor (BAF) was determined to quantify bioaccumulation of the heavy metals in fish tissues, according to Sures et al. (Reference Sures, Siddall and Taraschewski1999).

All values from chemical analyses were presented as mean ±  SE. Data obtained from the experiment were subjected to one-way analysis of variance (ANOVA) test using the Statistical Package for the Social Sciences, v. 10, 1998 (SPSS, Chicago, Illinois, USA) after the logarithmic transformation was done on the data to improve normality, followed by Duncan's multiple range test as a multiple comparison procedure to assess whether the means of metal concentrations varied significantly among fish species. P values < 0.05 were considered statistically significant.

Results

Adult specimens of P. clarias were found in the upper part of the intestine in all fish examined; with a prevalence of 38% and a mean intensity of 5.53. The infection was increased during winter to 92.0% (23 out of 25), compared to 60.0% (15 out of 25) during summer, with no records in other seasons.

Taxonomic summary

Parasite name. Polyonchobothrium clarias Woodland, Reference Woodland1925; family Ptychobothriidae Luhe, 1902.

Host type. African sharptooth catfish Clarias gariepinus Burchell, 1822; family Clariidae Bonaparte, 1846.

Site of infection. Located in the upper portion of the intestine of the infected fish.

Locality. Lake Manzala, Dakahlia Governorate, Egypt.

Prevalence and mean intensity. (38 out of 100) and 5.53.

Etymology. The specific name of the parasite is derived from Clarias which is the generic name for the host fish from which the parasite was isolated for the first time.

Material deposition. Voucher specimens were deposited in the Zoology Department, Faculty of Science, Cairo University, Cairo, Egypt.

Microscopical examination

The adult worm (figs 2–4) was somewhat contracted, grey to whitish opaque in colour, and measured 7.23–27.31 (9 ± 0.1) mm in length, with a total number of proglottids ranging from 51 to 175 (130). The scolex was rectangular with a flat to slightly raised rostellum armed with a crown of 26–30 (28) hooks. It measured 0.43–0.58 (0.49 ± 0.1) mm long and 0.15–0.21 (0.19 ± 0.1) mm wide. The rostellum was divided into two semicircles each bearing 13–15 hooks. Hooks at the end of each semicircle were smaller than the others. There were two longitudinally elongated bothria in line with gaps between the crowns of hooks. There was no neck where the scolex was followed directly by the immature proglottids, about 29–55 (45) in number and measuring 0.071–0.092 (0.081 ± 0.01) mm in length and 0.137–0.167 (0.154 ± 0.1) mm in width; then the mature proglottids, each containing a single set of genitalia, were about 16–30 (24) in number, measuring 0.119–0.142 (0.128 ± 0.1) mm in length and 0.124–0.158 (0.129 ± 0.1) mm in width. Testes were medullary in two lateral fields, oval in shape, ranging from 25 to 55 in number per proglottid and each measuring 0.09–0.13 (0.11 ± 0.01) mm long and 0.05–0.08 (0.06 ± 0.01) mm wide. The ovaries were large in size, distinctly bi-lobed, situated near the posterior margin of the proglottid, extending laterally up to the longitudinal excretory canals. The isthmus was short, wide, connecting the two ovarian lobes. Ootype was large in size, round in shape, postero-ventral to the ovary and isthmus, near the posterior margin of the proglottid. Vitelline follicles were cortical, in lateral bands dorsally and ventrally, occasionally continuous around lateral margins of the proglottid. The longitudinal excretory canals were of medium width. Uterus was tubular, arising from the ootype, and extending anteriorly, up to the anterior margin of the proglottid. The gravid proglottids were about 15–39 (28) in number, measured 0.22–0.48 (0.31 ± 0.1) mm and 0.29–0.61 (0.57 ± 0.1) mm in length and width, respectively, and the greater portion – occupied by the uterus – was filled with eggs. The mature eggs were unoperculate and embryonated.

Fig. 2

The morphology of P. clarias to show an adult worm: (a) with rectangular scolex (SC), rostellum armed with hooks (HO), bothria followed by immature (IM), mature (M) and gravid (G) proglottids; (b) scolex (SC), rostellum (R), hooks (HO), bothria (B) and immature proglottid (IM); (c) rostellum (R) armed with a crown of hooks (HO); (d) high magnifications of hooks (HO); (e) immature proglottid (IM); (f) mature proglottid (M) with ovary (OV), uterus (U) filled with a few eggs (EG); (g) early stage of gravid proglottid (G) with ovary (OV), uterus (U) and eggs – note the presence of vitelline follicles (VF); (h) later stage of gravid proglottid (G) with uterus and numerous eggs (EG), and excretory canal (EC); (i) grouping of eggs (EG); (j) mature egg with hexacanth embryo (HE) surrounded by eggshell (ES).

Fig. 3

The morphology of P. clarias to show an adult worm: (a) with scolex (SC), rostellum, hooks (HO), bothria (B), immature (IM), mature (M) and gravid (G) proglottids; (b) scolex (SC) with rostellum (R), hooks (HO), bothria (B) and immature proglottid (IM); (c, d) hooks (HO); (e) mature proglottid (M) with ovary (OV), ootype (OO), uterus (U) opening via uterine pore (UP), genital atrium (GA) opening via genital pore (GP), vitelline follicles (VF), testes (TE), excretory canal (EC); (f) gravid proglottid (G) with uterus (U) filled with numerous eggs (EG), and excretory canal (EC); (g) mature egg with hexacanth embryo (HE) surrounded by eggshell (ES).

Fig. 4

Scanning electron microscopy of P. clarias to show an adult worm: (a) with scolex (SC), rostellum (R), hooks (HO), bothria (B), immature (IM) and mature (M) proglottids; (b, c, d) scolex (SC), rostellum (R), hooks (HO) and bothria (B); (e) immature proglottid (IM); (f) mature proglottid (M); (g) gravid proglottid (G).

Chemical analyses

The concentrations (μg/g) of the trace metals in the host–parasite system are shown in table 1. Mean concentrations of heavy metals in fish decrease in the order: Zn > Cu > Mn > Cd > Pb > Ni. Considering the mean concentrations of accumulated heavy metals, the kidney was found to be a key target organ, followed by the liver and muscles. Zinc was the dominant element in all of the evaluated fish tissues. Large quantities of Zn can accumulate in the kidney, higher than those in the remaining tissues. The liver represented the main site for Cu accumulation, while the highest amounts of Pb and Mn were found in the muscles, and Cd was predominant in the liver and kidney. Concentrations of the heavy metals detected in parasites were higher than those in the tissues of host fish, with the exception of Zn, which was found at higher levels in fish kidneys than in the parasite tissues. In addition, the bioaccumulation factor indicated that the concentration of the heavy metals in different tissues of fish were higher than those in water (table 2).

Table 1

Mean heavy metal concentrations (mg/g wet weight ± SE) in the liver, kidney and muscles of fish, together with mean values for P. clarias (± SE).

Table 2

Estimates of the bioaccumulation factor of heavy metals in the liver, kidney and muscle of fish infected with P. clarias and uninfected fish.

Discussion

Lake Manzala is the largest of the northern deltaic lakes of Egypt and served as a significant source of inexpensive fish for human consumption in Egypt, but pollution and lake drainage have reduced the lake's productivity. Fish frequently serve as intermediate or transport hosts for larval parasites of many animals, including humans (Negm-El Din, Reference Negm-El Din1987; Abu El-Ezz, Reference Abu El-Ezz1988; Faisal & Shalaby, Reference Faisal and Shalaby1989; Galli et al., Reference Galli, Crosa and Occhipinti Ambrogi1998; Abdel-Gaber et al., Reference Abdel-Gaber, El Ghary and Morsy2015). In general, heavy parasite burdens seem to be more common in fish originating from wild sources (Merck Veterinary Manual, 2006). Polyonchobothrium clarias is a widely distributed cestode parasite in African freshwater siluroid fish, having been recorded from C. gariepinus Burchell, 1822 in the River Nile in Egypt (Imam, Reference Imam1971; Bassiony, Reference Bassiony2002; Eissa et al., Reference Eissa, Badran, Sohair, Mohamed and Abdelmola2010), C. lazera Cuvier and Valenciennes, 1840 in Nigeria (Aderounmu & Adeniyi, Reference Aderounmu and Adeniyi1972), Heterobranchus bidorsalis Geoffroy Saint-Hilaire, 1809 from Senegal (Khalil, Reference Khalil1973), C. gariepinus in seven dams in the Lebowa region, Limpopo Province, South Africa (Mashego, Reference Mashego1977), Bagrid catfish Chrysichthys thonneri Steindachner, 1912 from Gabon, and the mud-fish C. anguillaris Linnaeus, 1758 from Egypt (Amin, Reference Amin1978). In the present study, the African catfish C. gariepinus was found to be naturally infected with P. clarias, with a prevalence of 38.0%. These results coincide with data obtained by Imam (Reference Imam1971) who reported an incidence of P. clarias as high as 42.0% for C. gariepinus dwelling in the Nile in mid Egypt (Cairo and Giza Provinces), while a prevalence of 22% in Lake Manzala, Egypt has also been recorded. In addition, Bassiony (Reference Bassiony2002) and Eissa et al. (Reference Eissa, Badran, Sohair, Mohamed and Abdelmola2010) recorded that the highest infestation rate of C. gariepinus with P. clarias was recorded in winter, and the lowest rate occurred in summer; these data coincide with our results.

Morphological and morphometric descriptions of the present mature cestode parasite were identical to P. clarias Woodland, Reference Woodland1925, having all the characteristics described by Yamaguti (Reference Yamaguti1959) for the genus Polyonchobothrium – a nearly rectangular scolex with hooks arranged in four quadrants, two longitudinally elongated bothria in line with the gaps between the crowns of hooks, followed by a number of proglottids, eggs embryonated – and the dimensions of the body parts being more or less similar. These findings were closely similar to the previous descriptions for P. clarias given by Barson & Avenant-Oldewage (Reference Barson and Avenant-Oldewage2006) and Mohammed (Reference Mohammed2012) (table 3). Our observations for live specimens of P. clarias in the current study found that they differed from those described by Saayman et al. (Reference Saayman, Mashego, Mokgalong, Saayman, Schoonbee and Smit1991) only in that the material described by the latter authors had a triangular scolex and some specimens were found in the main bile duct of the host, which they described as ‘more robust’ than the intestinal specimen. In addition, our observations differ from those reported for P. ophiocephalina from Chinese perch (Zhongzhang, Reference Zhongzhang1982) and P. magnum from Russia (Bykhovskaya-Pavlovskaya et al., Reference Bykhovskaya-Pavlovskaya, Gusev, Dubinina, Izyumovan, Smirnova, Sokolskaya, Shtein, Shulman and Epstajn1962) by having a conical scolex and a trapezoidal scolex, respectively. Also, Saayman et al. (Reference Saayman, Mashego, Mokgalong, Saayman, Schoonbee and Smit1991) reported that the scolex apex (rostellum) is distinctly elevated, which differs from our specimens which show a more or less flattened rostellum. The scolex of the present specimens was provided with a circle of 32 hooks arranged in four quadrants of eight hooks each, and more closely resembles other species described by Barson & Avenant-Oldewage (Reference Barson and Avenant-Oldewage2006) and Mohammed (Reference Mohammed2012), while it differs significantly from those of species infecting fish in Nigeria (30; Aderounmu & Adeniyi, Reference Aderounmu and Adeniyi1972) and Zimbabwe (38; Chishawa, Reference Chishawa1991).

Table 3

Comparative morphometrics (in mm) of P. clarias from Egypt with previous descriptions by Barson & Avenant-Oldewage (Reference Barson and Avenant-Oldewage2006) and Mohammed (Reference Mohammed2012).

Lake Manzala is one of the most heavily polluted areas on the Egyptian Mediterranean coast, receiving huge amounts of agricultural, industrial and sewage waste (Abdalla et al., Reference Abdalla, Zaghloul, Hassan and Moustafa1995; Ansari et al., Reference Ansari, Gill, Lanza and Rast2011). Certain organisms are able to provide information about the chemical state of their environment through their presence or absence (Schäperclaus, Reference Schäperclaus1990; Sures, Reference Sures2008; Marcogliese et al., Reference Marcogliese, King, Salo, Fournier, Brousseau, Spear, Champoux, McLaughlin and Boily2009). Others are less affected by toxic substances but show an ability to concentrate environmental pollutants inside their tissues (Rosenberg & Resh, Reference Rosenberg and Resh1993; Sures et al., Reference Sures, Scheef, Klar, Kloas and Taraschewski2002; Marcogliese et al., Reference Marcogliese, Dautremepuits, Gendron and Fournier2010). It is well known that copper, manganese, nickel and zinc are essential elements required by a wide variety of enzymes and other cell components, and having vital functions in all living organisms, but very high intakes can cause adverse health problems (Demirezen & Uruc, Reference Demirezen and Uruc2006; Elnabris et al., Reference Elnabris, Muzyed and El-Ashgar2013). On the other hand, Cd and Pb have no biological role and hence they are harmful to living organisms even at considerably low concentrations. In this study, the overall average concentrations of metals were found to accumulate in the order of Zn > Cu > Mn > Cd > Pb > Ni, with concentrations of essential elements being higher than those of non-essential elements. These results may confirm the essential role of the former metals to fish species. Although it is not always the rule, these results agreed with the observations of Chen & Chen (Reference Chen and Chen2001) (Zn =  Fe > Cu =  Mn > Cd) and Bahnasawy et al. (Reference Bahnasawy, Khidr and Dheina2009) (Zn > Cu > Pb > Cd). The current investigation demonstrated that the distribution of Zn in different organs of infected fish followed the order: kidney > muscles > liver, these results agreed with data obtained by Pourang (Reference Pourang1995) who studied the accumulation of different heavy metals in Esox lucius and Carassius auratus from Anzali wetland. This investigation shows that the kidney represents a key target organ, receiving the largest quantities of heavy metals from the body. On the other hand, Cu and Cd take the following order: liver > kidney > muscles. This is in agreement with WHO–IPCS–Environmental Health Criteria (1987) which reported that the liver is considered the second most important heavy-metal storage organ as it accumulates higher concentrations of Cu and Cd compared to the other fish tissues. The current investigation reported that infected fish contain low concentrations of heavy metals in their tissues as compared to non-infected fish. In addition, the metal concentrations of P. clarias were compared to those of different organs of its host, showing that it accumulates heavy metals at concentrations that are orders of magnitude higher than those in their fish hosts. These results agreed with those of Madanire-Moyo & Barson (Reference Madanire-Moyo and Barson2010), who confirmed that cestode parasites seem to be good indicators of environmental conditions.

This recent field study includes a re-description of P. clarias infecting C. gariepinus inhabiting Egyptian freshwater. In addition, it demonstrated that particular fish cestode parasites can accumulate toxic metals from the aquatic environment more than their hosts. Thus, the application of certain parasites as sentinel organisms could provide a promising new domain for future research into environmental issues.

Acknowledgements

The authors extend their appreciation to the Faculty of Science, Cairo University, Cairo, Egypt, for providing all facilities to complete this work.

Conflict of interest

None.

Ethical standards

Animal use followed a protocol approved and authorized by the Institutional Animal Care and Use Committee (IACUC) of the Faculty of Science, Cairo University, Egypt.

References

Abdalla, R.R., Zaghloul, F.A., Hassan, Y.A. & Moustafa, H.M. (1995) Effects of industrial wastes on the chemical characteristics of the Eastern Harbour and El-Mex Bay waters of Alexandria, Egypt. Proceedings of the International Conference on Marine Coastal Eutrophication, Bologna, Italy 21, 773–784.Google Scholar
Abdel-Gaber, R., El Ghary, M. & Morsy, K. (2015) Prevalence and intensity of helminth parasites of African catfish Clarias gariepinus in Lake Manzalah, Egypt. Advances in Bioscience and Biotechnology 6, 464–469.CrossRefGoogle Scholar
Abdel-Ghaffar, F., Abdel-Gaber, R., Bashtar, A.R., Morsy, K., Mehlhorn, H., Al Quraishy, S. & Saleh, R. (2014) Hysterothylacium aduncum(Nematoda, Anisakidae) with a new host record from the common sole Solea solea(Soleidae) and its role as a biological indicator of pollution. Parasitology Research 114, 513–522.Google Scholar
Abu El-Ezz, N.M. (1988) Morphological studies on some gastrointestinal parasites of fresh water fish. MSc thesis, Faculty of Veterinary Medicine, Cairo University, Egypt.Google Scholar
Aderounmu, E.A. & Adeniyi, F. (1972) Cestodes in fish from a pond at IIe-Ife, Nigeria. African Journal of Tropical Hydrobiology and Fisheries 2, 151–156.Google Scholar
Amin, O.M. (1978) Intestinal helminths of some Nile fish near Cairo, Egypt, with redescriptions of Camallanus kirandensis Baylis, 1928 (Nematoda) and Bothriocephalus aegyptiacus Rysavy and Moravec, 1975 (Cestode). Journal of Parasitology 64, 93–101.Google Scholar
Ansari, A.A., Gill, S.S., Lanza, G.R. & Rast, W. (2011) Eutrophication: causes, consequences and control. Dordrecht, Springer.Google Scholar
Awachie, J.B.E. & Ezenwaji, G.H.M. (1981) The importance of Clarias species in fisheries development of the Anambra River basin, Nigeria. CIFA Technical Paper 7, 212–224.Google Scholar
Bahnasawy, M., Khidr, A. & Dheina, N. (2009) Seasonal variations of heavy metal concentrations in mullet, Mugil cephalus and Liza ramada (Mugilidae) from Lake Manzala, Egypt. Journal of Applied Science Research 5, 845–852.Google Scholar
Bahnasawy, M., Khidr, A. & Dheina, N. (2011) Assessment of heavy metal concentrations in water, plankton, and fish of Lake Manzala, Egypt. Turkish Journal of Zoology 35, 271–280.Google Scholar
Barson, M. & Avenant-Oldewage, A. (2006) On cestode and digenean parasites of Clarias gariepinus (Burchell, 1822) from the Rietviel Dam, South Africa. Onderstepoort Journal of Veterinary Research 73, 101–110.Google Scholar
Bassiony, A.E. (2002) Studies on the prevailing internal parasitic diseases among some cultured freshwater fish in Kafr El-Sheikh province. MSc thesis, Faculty of Veterinary Medicine, Tanta University, Egypt.Google Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Bykhovskaya-Pavlovskaya, I.E., Gusev, A.V., Dubinina, M.N., Izyumovan, A., Smirnova, T.C., Sokolskaya, I.L., Shtein, G.A., Shulman, S.S. & Epstajn, V.M. (1962) The guide for determination of parasites of fresh water fish of SSSR. Leningrad, Akademiya Nauk SSSR. Zoologicheskij Institut.Google Scholar
Chen, Y. & Chen, M. (2001) Heavy metal concentrations in nine species of fishes caught in coastal waters off Ann-Ping, S.W. Taiwan. Journal of Food Drug Analysis 9, 107–114.Google Scholar
Chishawa, A.M.M. (1991) A survey of the parasites of three Siluriforme fish species in Lake Kariba. University Lake Kariba Research Station Bulletin 1/91.Google Scholar
Demirezen, D. & Uruc, K. (2006) Comparative study of trace elements in certain fish, meat and meat products. Meat Science 74, 255–260.Google Scholar
Dural, M., Genc, E., Sangun, M.K. & Güner, Ö. (2011) Accumulation of some heavy metals in Hysterothylacium aduncum (Nematoda) and its host sea bream, Sparus aurata (Sparidae) from North-Eastern Mediterranean Sea (Iskenderun Bay). Environmental Monitoring and Assessment 174, 147–155.Google Scholar
Eissa, I.A.M., Badran, A.F., Sohair, Y., Mohamed, A. & Abdelmola, H. (2010) Entero-parasitic infestation and the associated pathological lesions in Clarias gariepinus at Ismailia province. Journal of Agricultural and Veterinary Science, Qassim University 3, 21–32.Google Scholar
Elnabris, K.J., Muzyed, S.K. & El-Ashgar, N.M. (2013) Heavy metal concentrations in some commercially important fishes and their contribution to heavy metal exposure in Palestinian people of Gaza Strip (Palestine). Journal of the Association of Arab Universities for Basic and Applied Sciences 13, 44–51.Google Scholar
Faisal, M. & Shalaby, S.I. (1989) Helminthic parasites of the African Cat Fish Clarias lazera in Lower Egypt Polyonchobothrium clarias . Wozeitschrift-furAngewandte-Zoologie 76, 177–188.Google Scholar
FAO/WHO. (2004) Summary of evaluations performed by the Joint FAO/WHO Expert Committee on Food Additives (JECFA 1956–2003), (First Through Sixty First Meetings). Washington, DC, ILSI Press.Google Scholar
Galli, P., Crosa, G. & Occhipinti Ambrogi, A. (1998) Heavy metal concentrations in acanthocephalan parasites compared to their fish host. Chemosphere 37, 2983–2988.Google Scholar
Hassan, M.H.A. (1992) Studies on some parasitic infections in freshwater fish in Beni-Suef Governorate. PhD thesis (Parasitology), Faculty of Veterinary Medicine, Cairo University, Egypt.Google Scholar
Idodo-Umeh, G. (2003) Fresh-water fishes of Nigeria: Taxonomy, ecological notes, diet and utilization. Nigeria, Idodo-Umeh Publishers.Google Scholar
Imam, E.A.E. (1971) Morphological and biological studies of the enteric helminthes infesting some of the Egyptian Nile fish, particularly Polyonchobothrium clarias of the Karmotes Clarias lazera and Clarias anguillaris . MSc thesis, Faculty of Veterinary Medicine, Cairo University, Egypt.Google Scholar
Innes, W.T. (1966) Exotic aquarium fishes. 19th edn. New Jersey, Aquarium Incorporated.Google Scholar
Janicki, C. (1926) Cestodes s. str. aus Fischen u. Amphibien. pp. 222–223 in Jägerskiöld, L.A. (Ed.) Results of the Swedish Zoological Expedition to Egypt and the White Nile 1901. Part V. The Library of the Royal University of Uppsala.Google Scholar
Khalil, L.F. (1973) Some helminth parasites from African freshwater fish with the description of two new species. Revue de Zoologie et de Botanique Africaines 87, 795–807.Google Scholar
Leydig, F. (1853) Ein neuer Bandwurm aus Polypterus bichir . Archivfur Naturgeschichte 19, 219–222.Google Scholar
Madanire-Moyo, G.N. & Barson, M. (2010) Diversity of metazoan parasites of the African catfish Clarias gariepinus (Burchell, 1822) as indicators of pollution in a subtropical African river system. Journal of Helminthology 84, 216–227.Google Scholar
Marcogliese, D.J., Brambilla, L.G., Gagne, F. & Gendron, A.D. (2005) Joint effects of parasitism and pollution on oxidative stress biomarkers in yellow perch Perca flavescens . Diseases of Aquatic Organisms 63, 77–84.Google Scholar
Marcogliese, D.J., King, K.C., Salo, H.M., Fournier, M., Brousseau, P., Spear, P., Champoux, L., McLaughlin, J.D. & Boily, M. (2009) Combined effects of agricultural activity and parasites on biomarkers in the bullfrog, Rana catasbeiana . Aquatic Toxicology 91, 126–134.Google Scholar
Marcogliese, D.J., Dautremepuits, C., Gendron, A.D. & Fournier, M. (2010) Interactions between parasites and pollutants in yellow perch (Perca flavescens) in the St. Lawrence River, Canada: implications for resistance and tolerance to parasites. Canadian Journal of Zoology 88, 247–258.Google Scholar
Mashego, S.N. (1977) A seasonal investigation of the ecto- and endoparasites of the barbel, Clarias gariepinus Burchell, 1822 in Lebowa, South Africa. MSc thesis, University of the North, South Africa.Google Scholar
Merck Veterinary Manual. (2006) Helminthiasis. Whitehouse Station, New Jersey, USA, Merck and Co. Inc. Published in educational partnership with Merial Ltd.Google Scholar
Mohammed, R.A. (2012) Critical role of Cyclops strenus in the biology of Polyonchobothrium clarias (Cestode) parasitizing cultured (Clarias garipenus). Egyptian Journal for Aquaculture 2, 93–103.Google Scholar
Negm-El Din, K.M. (1987) Some morphological studies on the internal parasites of fish Delta Nile. MSc thesis, Faculty of Veterinary Medicine, Zagzig University, Benha branch (Moshtohor), Egypt.Google Scholar
Olufemi, B.E., Akinlabi, D.A. & Agbede, S.A. (1991) Aerobic bacterial pathogens isolated from the African catfish Clarias gariepinus . Tropical Veterinarian 9, 177–180.Google Scholar
Oniye, S.J., Adebote, D.A. & Ayanda, O.I. (2004) Helminth parasites of Clarias gariepinus (Teugels) in Zaria, Nigeria. Journal of Aquatic Sciences 19, 71–76.Google Scholar
Paperna, I. (1996) Parasite infection and diseases of fish in Africa: An update . Technical Paper 31. Rome, Central Institute of Freshwater Aquaculture, Food and Agriculture Organization, United Nations.Google Scholar
Pourang, N. (1995) Heavy metal bioaccumulation in different tissues of two fish species with regards to their feeding habits and trophic levels. Environmental Monitoring and Assessment 35, 207–219.Google Scholar
Ramadan, R.A.M. (1994) Study on internal parasites of some species of fresh water fish. MSc thesis, Faculty of Veterinary Medicine, Suez Canal University, Egypt.Google Scholar
Rosenberg, D.M. & Resh, V.H. (1993) Freshwater biomonitoring and benthic macroinvertebrates. New York, Chapman & Hall.Google Scholar
Saayman, J.E., Mashego, S.N. & Mokgalong, N.M. (1991) Parasites of the fish population with notes on the helminth parasites of the water birds of Middle Letaba Dam. pp. 8.1–8.210 in Saayman, J.E., Schoonbee, H.J. & Smit, G.L. (Eds) A postimpoundment ecological study of the Middle Letaba Dam, Gazankulu. Pretoria, Department of Development Aid.Google Scholar
Schäperclaus, W. (1990) Fischkrankheiten, 5. Aufl. Berlin, Akademie Verlag.Google Scholar
Sures, B. (2008) Environmental parasitology. Interactions between parasites and pollutants in the aquatic environment. Parasite 15, 434–438.Google Scholar
Sures, B., Siddall, R. & Taraschewski, H. (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitology Today 15, 16–21.CrossRefGoogle ScholarPubMed
Sures, B., Scheef, G., Klar, B., Kloas, W. & Taraschewski, H. (2002) Interaction between cadmium exposure and infection with the intestinal parasite Moniliformis moniliformis (Acanthocephala) on the stress hormone levels in rats. Environmental Pollution 119, 333–340.Google Scholar
Tadros, G. (1966) On the classification of the family Bothriocephalidae Blanchard, 1849 (Cestode). Journal of Veterinary Science of the United Arab Republic 3, 39–43.Google Scholar
UNEP/FAO/IOC/IAEA. (1984) Sampling of selected marine organisms and sample preparation for trace metal analysis: Reference methods for marine pollution studies. Revision 2, 19.Google Scholar
Wedl, K. (1861) Zur Helminthen fauna Aegyptens. Sitzungsberichte aus der Kaiserliche Akademie der Wissenschaften 44, 463–482.Google Scholar
WHO–IPCS–Environmental Health. (1987) International program of chemical safety. WHO–IPCS–Environmental Health Criteria Report, with ILO and UNEP. Geneva, Switzerland, WHO.Google Scholar
Woodland, J. (2006) National wild fish health survey – laboratory procedures manual. 3.1 edn. Pinetop, Arizona, US, Fish and Wildlife Service.Google Scholar
Woodland, W.N.F. (1925) Tetracampos Wedl, 1861 as a genus of the Bothriocephalidae. Annals of Tropical Medicine and Parasitology 19, 158–189.Google Scholar
Yamaguti, S. (1959) Systema Helminthum Vol. II. The cestodes of vertebrates. New York, Interscience.Google Scholar
Yamaguti, S. (1961) Systema Helminthum Vol. III. The nematodes of vertebrates. Parts I and II. New York, Interscience.Google Scholar
Zhongzhang, T. (1982) Developmental studies on Polyonchobothrium ophiocephalina (Tseng 1933) and Bothriocephalus opsariichthydis Yamaguti, 1934. Acta Zoologica Sinica 28, 51–59.Google Scholar
Figure 0

Fig. 1Geographical location of Lake Manzala, Dakahlia province, Egypt.

Figure 1

Fig. 2The morphology of P. clarias to show an adult worm: (a) with rectangular scolex (SC), rostellum armed with hooks (HO), bothria followed by immature (IM), mature (M) and gravid (G) proglottids; (b) scolex (SC), rostellum (R), hooks (HO), bothria (B) and immature proglottid (IM); (c) rostellum (R) armed with a crown of hooks (HO); (d) high magnifications of hooks (HO); (e) immature proglottid (IM); (f) mature proglottid (M) with ovary (OV), uterus (U) filled with a few eggs (EG); (g) early stage of gravid proglottid (G) with ovary (OV), uterus (U) and eggs – note the presence of vitelline follicles (VF); (h) later stage of gravid proglottid (G) with uterus and numerous eggs (EG), and excretory canal (EC); (i) grouping of eggs (EG); (j) mature egg with hexacanth embryo (HE) surrounded by eggshell (ES).

Figure 2

Fig. 3The morphology of P. clarias to show an adult worm: (a) with scolex (SC), rostellum, hooks (HO), bothria (B), immature (IM), mature (M) and gravid (G) proglottids; (b) scolex (SC) with rostellum (R), hooks (HO), bothria (B) and immature proglottid (IM); (c, d) hooks (HO); (e) mature proglottid (M) with ovary (OV), ootype (OO), uterus (U) opening via uterine pore (UP), genital atrium (GA) opening via genital pore (GP), vitelline follicles (VF), testes (TE), excretory canal (EC); (f) gravid proglottid (G) with uterus (U) filled with numerous eggs (EG), and excretory canal (EC); (g) mature egg with hexacanth embryo (HE) surrounded by eggshell (ES).

Figure 3

Fig. 4Scanning electron microscopy of P. clarias to show an adult worm: (a) with scolex (SC), rostellum (R), hooks (HO), bothria (B), immature (IM) and mature (M) proglottids; (b, c, d) scolex (SC), rostellum (R), hooks (HO) and bothria (B); (e) immature proglottid (IM); (f) mature proglottid (M); (g) gravid proglottid (G).

Figure 4

Table 1Mean heavy metal concentrations (mg/g wet weight ± SE) in the liver, kidney and muscles of fish, together with mean values for P. clarias (± SE).

Figure 5

Table 2Estimates of the bioaccumulation factor of heavy metals in the liver, kidney and muscle of fish infected with P. clarias and uninfected fish.

Figure 6

Table 3Comparative morphometrics (in mm) of P. clarias from Egypt with previous descriptions by Barson & Avenant-Oldewage (2006) and Mohammed (2012).