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Sclerocollum saudii Al-Jahdali, 2010 (Acanthocephala: Cavisomidae) as a sentinel for heavy-metal pollution in the Red Sea

Published online by Cambridge University Press:  07 February 2018

R.M. El-S. Hassanine*
Affiliation:
Biological Sciences Department, Rabigh-Faculty of Science and Arts, King Abdulaziz University, PO Box 344, Rabigh 21911, Saudi Arabia Department of Zoology, New Valley-Faculty of Science, Assiut University, El-Kharga, New Valley, Egypt
Z.M. Al-Hasawi
Affiliation:
Biological Sciences Department, Rabigh-Faculty of Science and Arts, King Abdulaziz University, PO Box 344, Rabigh 21911, Saudi Arabia
M.S. Hariri
Affiliation:
Biological Sciences Department, Rabigh-Faculty of Science and Arts, King Abdulaziz University, PO Box 344, Rabigh 21911, Saudi Arabia
H. El-S. Touliabah
Affiliation:
Biological Sciences Department, Rabigh-Faculty of Science and Arts, King Abdulaziz University, PO Box 344, Rabigh 21911, Saudi Arabia
*
Author for correspondence: R.M. El-S. Hassanine, E-mail: redaaa2003@yahoo.com

Abstract

Currently, fish helminth parasites, especially cestodes and acanthocephalans, are regarded as sentinel organisms to elucidate metal pollution in aquatic ecosystems. Here, 34 specimens of the fish Siganus rivulatus were collected in the Red Sea, from a seriously polluted, small lagoon named Sharm-Elmaya Bay, at Sharm El-Sheikh, South Sinai, Egypt; 22 (64.7%) were infected by Sclerocollum saudii (Acanthocephala: Cavisomidae). Thus, 22 natural infrapopulations (26–245 individuals) of this parasite were collected from infected fish. Samples of water and sediments from the bay, samples of muscle, intestine and liver from each fish, and samples from the parasite were taken for analysis of heavy metals (cadmium (Cd) and lead (Pb)). Both Cd and Pb concentrations in sediments were higher than those in water. The concentration of these metals were significantly higher in tissues (intestine, liver and muscle) of non-infected fish than those in infected fish, with Pb concentrations consistently higher than those of Cd, and both were drastically decreased in the order: liver > intestine > muscle. Metal concentrations in this acanthocephalan were much higher than those in its fish host. There were strong negative relationships between metal concentrations in tissues (intestine, liver and muscle) of infected fish and infrapopulation size, and between metal concentrations in the acanthocephalan and its infrapopulation size. These relationships strongly suggest competition for these metals between the fish host and its acanthocephalan parasite, and intraspecific competition among acanthocephalan individuals for available metals in the fish intestine. Bioconcentration factors were relatively high, since the mean Cd concentration in S. saudii was 239, 68 and 329 times higher than those in intestine, liver and muscle tissues, respectively, of its fish host. Also, mean Pb concentration was 55, 13 and 289 times higher than those in these tissues, respectively. The host–parasite system described here seems to be promising for biomonitoring of metal pollution in the Red Sea.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2018 

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References

Al-Jahdali, MO and Hassanine, RM El-S (2012) Infrapopulations of Sclerocollum saudii Al-Jahdali, 2010 (Acanthocephala: Cavisomidae) in the rabbitfish Siganus rivulatus (Teleostei, Siganidae) from the Saudi coast of the Red Sea. Journal of Helminthology 86, 8594.Google Scholar
Al-Jahdali, MO, Hassanine, RM El-S and Touliabah, H El-S (2015) The life cycle of Sclerocollum saudii Al-Jahdali, 2010 (Acanthocephala: Palaeacanthocephala: Rhadinorhynchidae) in amphipod and fish hosts from the Red Sea. Journal of Helminthology 89, 277287.Google Scholar
Al-Saadi, HA, Al-Lami, AA, Hassan, FA and Aldulymi, AA (2002) Heavy metals in water, suspended particles, sediments and aquatic plants of Habbaniya Lake, Iraq. International Journal of Environmental Studies 59, 589598.Google Scholar
Al-Yousuf, MH, El-Shahawi, MS and Al-Ghais, SM (2000) Trace elements in liver, skin and muscle of Lethrinus lentjan fish species in relation to body length and sex. The Science of the Total Environment 256, 8794.Google Scholar
Bayoumy, EM, Osman, HAM, El-Bana, LF and Hassanain, MA (2008) Monogenean parasites as bioindicators for heavy metals status in some Egyptian Red Sea fishes. Global Veterinaria 2, 117122.Google Scholar
Brázová, T, Hanzelová, V, Miklisová, D, Šalamún, P and Vidal-Martínez, VM (2015) Host–parasite relationships as determinants of heavy metal concentrations in perch (Perca fluviatilis) and its intestinal parasite infection. Ecotoxicology and Environmental Safety 122, 551556.Google Scholar
Buckley, JT, Roch, M, McCarter, JA, Rendell, CA and Matheson, AT (1982) Chronic exposure of Coho salmon to sublethal concentration of copper. Effect on growth, on accumulation and distribution of copper and on copper tolerance. Comparative Biochemistry and Physiology 72C, 1519.Google Scholar
Carpene, E and Vašák, M (1989) Hepatic metallothioneins from goldfish (Carassius auratus). Comparative Biochemistry and Physiology 92B, 463468.Google Scholar
Dauvalter, VA (1998) Heavy metals in the bottom sediments of the Inari-Pasvik lake–river system. Water Resources 25, 451457.Google Scholar
Deb, SC and Fukushima, T (1999) Metals in aquatic ecosystems: mechanisms of uptake, accumulation and release: ecotoxicological perspectives. International Journal of Environmental Studies 56, 385417.Google Scholar
Diamant, A (1989) Ecology of the acanthocephalan Sclerocollum rubrimaris Schmidt and Paperna, 1978 (Rhadinorhynchidae: Gorgorhynchinae) from wild populations of rabbitfish (genus Siganus) in the northern Red Sea. Journal of Fish Biology 34, 387398.Google Scholar
Egyptian Environmental Affairs Agency (EEAA) (2003) Marine pollution in the Gulf of Aqaba and Gulf of Suez and its effects on South Sinai. A comprehensive review. Available at http://st-katherine.net/en/downloads/Marine%20Pollution.pdf (accessed 26 January 2018).Google Scholar
Eira, C, Torres, J, Miquel, J, Vaqueiro, J, Soares, AM and Vingada, J (2009) Trace element concentrations in Proteocephalus macrocephalus (Cestoda) and Anguillicola crassus (Nematoda) in comparison to their fish host, Anguilla anguilla in Ria de Aveiro. Portugal Science of the Total Environment 407, 991998.Google Scholar
Eneji, IS, Ato, RS and Annune, PA (2011) Bioaccumulation of heavy metals in fish (Tilapia zilli and Clarias gariepinus) organs from River Benue, North Central Nigeria. Pakistan Journal of Analytical and Environmental Chemistry 12, 2531.Google Scholar
Goater, TM, Goater, CP and Esch, GW (2013) Parasitism: the diversity and ecology of animal parasites. Cambridge, Cambridge University Press.Google Scholar
Grahl, K (1990) Erkennung von Schadstoffeinflussen auf die Gesundheit von Fischen mittels Gallendiagnostik. pp. 240243 in DVG/Fachgruppe. Fischkrankheiten: Tagung der Fachgruppe Fischkrankheiten, Schmiedefeld/Thüringen, Germany, November.Google Scholar
Hassan, AH, Al-Zanbagi, NA and Al-Nabati, EA (2016) Impact of nematode helminthes on metal concentrations in the muscles of Koshar fish, Epinephelus summana, in Jeddah, Saudi Arabia. The Journal of Basic and Applied Zoology 74, 5661.Google Scholar
Hassanine, RM and Al-Jahdali, MO (2007) Ecological comments on the intestinal helminths of the rabbitfish Siganus rivulatus (Teleostei, Siganidae) from the northern Red Sea. Acta Parasitologica 52, 278285.Google Scholar
Hofer, R and Lackner, R (1995) Fischtoxikologie – Theorie und Praxis. Jena, Fischer Verlag.Google Scholar
Karadede, H and Ünlü, E (1998) Investigation of the heavy metal accumulation in Cyprinion macrostomus Heckel, 1843, (Cyprinidae) from The Atatürk Dam Lake: XIV. Turkish Biology Congress, Samsun-Turkey, 7–10 September.Google Scholar
Karadede, H and Ünlü, E (2000) Concentrations of some heavy metals in water, sediment and fish species from The Atatürk Dam Lake (Euphrates), Turkey. Chemosphere 41, 13711376.Google Scholar
Karadede, H, Oymak, SA and Ünlü, E (2004) Heavy metals in mullet, Liza abu, and catfish, Silurus triostegus, from the Atatürk Dam Lake (Euphrates), Turkey. Environment International 30, 183188.Google Scholar
Kargin, F and Erdem, C (1991) Accumulation of copper in liver, spleen, stomach, intestine, gill and muscle of Cyprinus carpio. Turkish Journal of Zoology 15, 306314.Google Scholar
Kennedy, CR (2006) Ecology of the Acanthocephala. 1st edn. Cambridge, Cambridge University Press.Google Scholar
Kennedy, CR, Broughton, PF and Hine, PM (1978) The status of brown trout, Salmo trutta and Salmo gairdneri as hosts of the acanthocephalan, Pomphorhynchus laevis. Journal of Fish Biology 13, 265275.Google Scholar
Khalil, M and Faragallah, H (2008) The distribution of some leachable and total heavy metals in core sediments of Manzala Lagoon, Egypt. Egyptian Journal of Aquatic Research 34, 111.Google Scholar
Kojima, Y and Kagi, JHR (1978) Metallothionein. Trends in Biochemical Sciences 3, 9093.Google Scholar
Luorna, SN (1990) Processes affecting metal concentrations in estuarine and coastal marine sediments. pp. 166 in Furness, RW and Rainbow, PS (Eds) Heavy metals in the marine environment. Florida, CRC Press.Google Scholar
Marzouk, M (1994) Fish and environment pollution. Veterinary Medicine Journal 42, 5152.Google Scholar
Mazhar, R, Shazili, NA and Harrison, FS (2014) Comparative study of the metal accumulation in Hysterothalycium reliquens (nematode) and Paraphilometroides nemipteri (nematode) as compared with their doubly infected host, Nemipterus peronii (Notched threadfin bream). Parasitology Research 113, 37373743.Google Scholar
Merian, E (2004) Elements and their compounds in the environment. Occurrence, analysis and biological relevance. Weinheim, Wiley.Google Scholar
Nachev, M (2010) Bioindication capacity of fish parasites for the assessment of water quality in the Danube River. PhD thesis, Universität Duisburg-Essen, Sofia, Bulgaria.Google Scholar
Nachev, M and Sures, B (2016) Environmental parasitology: parasites as accumulation bioindicators in the marine environment. Journal of Sea Research 113, 4550.Google Scholar
Nachev, M, Schertzinger, G and Sures, B (2013) Comparison of the metal accumulation capacity between the acanthocephalan Pomphorhynchus laevis and larval nematodes of the genus Eustrongylides sp. infecting barbel (Barbus barbus). Parasites & Vectors 6, 21.Google Scholar
Nickol, BB (1985) Epizootiology. pp. 307346 in Crompton, DWT and Nickol, BB (Eds) Biology of the Acanthocephala. Cambridge, Cambridge University Press.Google Scholar
Oregioni, B and Aston, SR (1984) The determination of selected trace metals in marine sediments by flameless/flame atomic absorption spectrophotometry. IAEA Manaco Laboratory, Internal Report.Google Scholar
Paller, VGV, Resurreccion, DJB, de la Cruz, CPP and Bandal, MZ (2016) Acanthocephalan parasites (Acanthogyrus sp.) of Nile tilapia (Oreochromis niloticus) as biosink of lead (Pb) contamination in a Philippine freshwater lake. The Bulletin of Environmental Contamination and Toxicology 96, 810815.Google Scholar
Poulin, R (2006) Evolutionary ecology of parasites. 2nd edn. Princeton, Princeton University Press.Google Scholar
Sasal, P, Jobet, E, Faliex, E and Morand, S (2000) Sexual competition in an acanthocephalan parasite of fish. Parasitology 120, 6569.Google Scholar
Schmidt, GD and Paperna, I (1978) Sclerocollum rubrimaris gen. et sp. n. (Rhadinorhynchidae: Gorgorhynchinae), and other Acanthocephala of marine fishes from Israel. Journal of Parasitolology 64, 846850.Google Scholar
Starling, JA (1985) Feeding, nutrition and metabolism. pp. 125212 in Crompton, DWT and Nickol, BB (Eds) Biology of the Acanthocephala. Cambridge, Cambridge University Press.Google Scholar
Sures, B (2002) Competition for minerals between Acanthocephalus lucii and its definitive host perch (Perca fluviatilis). International Journal of Parasitology 32, 11171122.Google Scholar
Sures, B (2003) Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126 (Suppl.), S53–60.Google Scholar
Sures, B (2004) Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20, 170177.Google Scholar
Sures, B and Siddall, R (1999) Pomphorhynchus laevis: the intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). Experimental Parasitology 93, 6672.Google Scholar
Sures, B and Taraschewski, H (1995) Cadmium concentrations in two adult acanthocephalans, Pomphorhynchus laevis and Acanthocephalus lucii, as compared with their fish hosts and cadmium and lead levels in larvae of A. lucii as compared with their crustacean host. Parasitology Research 81, 494497.Google Scholar
Sures, B, Taraschewski, H and Jackwerth, E (1994) Lead accumulation in Pomphorhynchus laevis and its host. Journal of Parasitology 80, 355357.Google Scholar
Sures, B, Siddall, R and Taraschewski, H (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitology Today 15, 1621.Google Scholar
Sures, B, Dezfuli, BS and Krug, HF (2003) The intestinal parasite Pomphorhynchus laevis (Acanthocephala) interferes with the uptake and accumulation of lead (210Pb) in its fish host chub (Leuciscus cephalus). International Journal of Parasitology 33, 16171622.Google Scholar
Sures, B, Nachev, M, Selbach, C, David, J and Marcogliese, DJ (2017) Parasite responses to pollution: what we know and where we go in ‘Environmental Parasitology’. Parasites & Vectors 10, 65.Google Scholar
Tekin-Ozan, S and Kir, İ (2008) Concentrations of some heavy metals in tench (Tinca tinca L., 1758), its endoparasite (Ligula intestinalis L., 1758), sediment and water in Beyşehir Lake, Turkey. Polish Journal of Environmental Studies 17, 597603.Google Scholar
Torres, J, Eira, C, Miquel, J, Ferrer-Maza, D, Delgado, E and Casadevall, M (2015) Effect of intestinal tapeworm Clestobothrium crassiceps on concentrations of toxic elements and selenium in European hake Merluccius merluccius from the Gulf of Lion (northwestern Mediterranean Sea). Journal of Agricultural and Food Chemistry 63, 93499356.Google Scholar
Yousafzai, AM, Khan, AR and Shakoori, AR (2009) Trace metal accumulation in the liver of an endangered South Asian fresh water fish dwelling in sub-lethal pollution. Pakistan Journal of Zoology 41, 3541.Google Scholar
Zimmermann, S, Menzel, C, Berner, Z, Eckhardt, JD, Stüben, D, Alt, F, Messerschmidt, J, Taraschewski, H and Sures, B (2001) Trace analysis of platinum in biological samples: a comparison between high resolution inductively coupled plasma mass spectrometry (HR-ICP-MS) following microwave digestion and adsorptive cathodic stripping voltammetry (ACSV) after high pressure ashing. Analytica Chimica Acta 439 (Suppl. 2), 203209.Google Scholar