Use of endoparasites, Ligula intestinalis plerercoid in ...
Use of endoparasites, Ligula intestinalis plerercoid in ... Use of endoparasites, Ligula intestinalis plerercoid in ...
Chromium showed site specific bioaccumulationby parasites showing higher concentration of metalcontent between parasites and host in site 2. This mayindicate environmental influence on the heavy metal,rather than the measured contents in fish that mayinterfere with the physiological functions of theparasites in the host. In site 2, we observed golddeposits along the river bed that may interfere with themetal accumulation in the fish. This variability, reflectthe mobility of the fish host and can obscure thedifferences that might be detected between sites.When the metal accumulation in fish parasitesand fish was compared in the enriched lake waterfrom site 1, the results are as shown in Tab. 3. Inenriched lake water, there was higher bioaccumulationof metals by a ranging from 10 times to 35.Bioaccumulation is a well documented field ofresearch (Rainbow, 2007; Zimmermann et al., 2004;Sizmur and Hodson, 2009). Normally,bioaccumulation of metals is through highly specificphysiological uptake mechanisms (Chapman, 1997;Rainbow, 2007) and reflects its exposure to pollutantsover time. Metals accumulate more rapidly than canbe eliminated due to low molecular weights, metalbinding proteins, such as metallothioneins (MT’s) andpresent in aquatic organisms. In addition, MT’scontrol the bioavailability and the kinetics ofbioaccumulation as well as the toxic effects that occurvia the induction of their biosynthesis (Baudrimont etal., 2003). For most fish, these intracellular proteinsbind specifically and have a high affinity for metals,such as Cd, Cu and Zn.In the aquatic environment, factors that canaffect bioaccumulation of metals include:environmental conditions, presence of specificbioavailable metal species (Rainbow and Dallinger,1993; Van Ginneken et al., 1999), trophic status ofbioaccumulation, physiological condition of theorganism, interactions between metals and the uptakeand release rates (kinetics) of metals by an organism(Buchwalter and Luoma, 2005). In fish-parasiteassociation, the normal physiological functioning offish is interrupted though it is not clear, which amongthese factors will exert great control over metals in thefish system.Metal concentration in L. intestinalis (mg kg -1 dw)the parasite tissues, albeit the increased Pb and Crcontent in parasite relative to the fish tissues was morepredictable than the changes in Cd (Fig. 3). Thissuggest an uptake of metal by parasites from the fishtissues as the metal content in R. argentea increasecomparable to the studies involving heavy metaluptake kinetics in parasites in fish tissues. On theother hand, increased Cu burden in the fish tissues wasassociated with linear reduction of the Cu in thetissues of the parasites. The present decline in Cu inparasite host as it increases in fish host was interpretedas elemental competition for essential element.Parasites and fish host have been shown to competefor several elements such as Ca, Cu, Fe, Zn and Sr inperch (Sures, 2002). Though there is paucity of dataon studies dealing with simultaneous analysis ofdifferent elements in fish, and even less studiesdealing with metal kinetic and metal metabolism infish-parasite association, it is probable thatcompetition for elements between host and parasitesfor essential elements could lead to increasedabsorption of other essential metals including Cu.Concentrations of Cu may be regulated by the fish aswell as by the parasite, albeit the physiologicallyrequired levels are actually higher in the parasite.These higher Cu concentrations should therefore notbe construed as bioaccumulation of environmentalpollutants.50.040.030.020.010.00.05.04.03.02.01.0Pb y = 3.6564x + 1.273R 2 = 0.57220.0 2.0 4.0 6.0 8.0 10.0Cr14.0y = 4.2418x + 0.9463R 2 = 0.60012.402.001.601.200.800.4012.010.08.0Cd y = 7.1748x + 0.3049R 2 = 0.4240.05 0.10 0.15 0.20 0.25Cuy = -0.9226x + 15.835R 2 = 0.4985Tab. 3 Heavy metal concentration in fish, parasite andthe overall bioaccumulation factor0.00.0 0.2 0.4 0.6 0.8 1.0 1.26.03.0 4.0 5.0 6.0 7.0 8.0Heavy metal concentrationBioconcentrationHeavymetals Fish Parasite factorPb36.22 ± 4.2 421.65 ± 10.2 11.6Cd0.78 ± 0.12 27.6 ± 1.92 35.4Cr3.95 ± 0.42 42.65 ± 1.44 10.8Cu11.01 ± 1.12 102.4 ± 5.55 10.2Increased content of Pb, Cd and Cr in R. argentearesulted to corresponding increase of these metals inFig. 3. Regression models showing the relationshipsbetween metal concentration (mg kg -1 dw) in L.intestinalis against metal concentration in Ligulaintestinalis4. ConclusionHeavy metal concentration in R. argentea (mg kg -1 dw)The present study shows that the L. intestinalis inR. argentea accumulates heavy metals in variablequantities in fish host. Some heavy metals such as Pb,Cd and Cr were bio accumulated by upto factor 11, 18and 14 respectively and Cu by factor 2.5 in the fish4
endoparasites in the natural water environment. Whenthe metal content in water within the experimentalunits containing fish and parasites were increased tenfoldthan metal concentration of the lake water in thelaboratory, all heavy metal concentrations in L.intestinalis increased between 10 to 35 time higherthan the concentration in tissues of its host. WhereasCu was demonstrated to be subject of elementcompetition between fish and parasite, Pb, Cd and Crdisplayed a partitioning in the fish host with parasiteshaving higher concentration of these metals, whichwould render the Ligula intestinalis in R. argenteahost a suitable as bio-monitor for exposure to thesemetals. It is evident that L. intestinalis is sensitiveindicator and early warning sign for increasing Pb, Cdand Cr pollution. Given that the parasite is easy toidentify even in different host (Olson et al. 2000;Tekin-Özan and Kir Tekin-Örzan and Barlas 2008), itshigh abundance and high prevalence, it was found tobe suitable bio-monitor model for early warning signfor localized pollution by Pb, Cd and Cr in LakeVictoria.AcknowledgmentsThe authors would like to thank the RoyalNetherlands Embassy in collaboration with VictoriaInstitute for Research on Environment andDevelopment (VIRED) International for funding thisproject. The LVEMP Project also provided additionalsupport to which we are grateful. The authors thankMr. Lewela of Moi University, Biochemical Analysislaboratory for the invaluable assistance in samplecollection and analysis of heavy metals.References[1] B. Sures, Accumulation of heavy metals by intestinalhelminths in fish, facts, appraisal and perspectives.Parasitol. 126: 53-60, 2003.[2] B. Sures, Environmental parasitology: relevancy ofparasites in monitoring environmental pollution. Trendsin Parasitol. 20(4): 170-177, 2004.[3] B. Sures, H. Taraschewski, and E. Jackwerth, Leadaccumulation in Pomphorhyncus laevis and its host. J.Parasitol. 80: 355-357, 1994a.[4] B. Sures, H. Taraschewski, and E. Jackwerth, Leadcontent of Paratenuisentis ambiguous (Acanthocephala),Anguillicola crassus (Nematodes) and their hostsAnguilla anguilla. Dis. Aquat. Org. 19: 105-107, 1994b.[5] B. Sures, H. Taraschewski. and E. Jackwerth,Comparative study of lead accumulation in differentorgans of perch (Perca fluviatilis) and its intestinalparasite Acanthocephalus lucii. Bull. Environ. Contam.Toxicol. 52: 269-273, 1994c.[6] B. Sures and H. Taraschewski, Cadmium concentrationin two adult acanthocephalans, Pomphorynchus laevisand Acanthocephalus lucii, as compared with their fishhosts and cadmium levels in larvae of A. lucii ascompared with their crustacean host. Parasitol. Res. 81:494-497, 1995.[7] B. Sures, R. Siddall. and H. Taraschewski, Parasites asaccumulation indicators of metal pollution. Internat. J.Parasitol. 33: 65-70. 1999.[8] J. Dvoracek, F. Tenora, V. Barus, and S. Kracmar,Concentrations of some heavy metals in Ligulaintestinalis plerocercoids (Cestoda) and Philometraovata (Nematoda) compared to some their hosts(Osteichthyes). Helminthol. 37(1):15-18, 2000.[9] B. Sures, The use of fish parasites as bioindicators ofheavy metals in aquatic ecosystems, a review. Aquat.Ecol. 35: 245-255, 2001.[10] C. Schludermann, S. Konecyny, S. Laimgruber, J.W.Lewis, F. Schiemer, A. Chovanec. and B. Sures, Fishmacroparasites as indicator of heavy metal pollution inriver sites in Austria. Parasitol. 126: 61-69, 2003[11] B. Sures and N. Reimann, Analysis of the trace metalsin the Antactic host-parasite system Nototheniacoriiceps and Aspersentis megarhynchus(Acanthocephala) caught at King George Island, SouthShetland Islands. Polar Biol. 26: 680-686, 2003.[12] F. Thielen, S. Zimmermann, F. Baska, H. Taraschewski,and B. Sures, The intestinal parasite Pomphorhyncuslaevis (Acanthocephala) from barbel as bioindicator formetal pollution in the Danube River near Budapest,Hungary. Environ. Pollut. 129: 420-429, 2004.[13] B. Sures, Host-parasite interactions from anecotoxicological perspective. Parasitol. 47(3): 173-176,2007.[14] S. Tekin-Özan and I. Kir, Comparative study on theaccumulation of heavy metals in different 291 organsof tench (Tinca tinca L. 1758) and plerocercoids of itsendoparasite Ligula intestinalis. Parasitol. Res. 97:156-69, 2005.[15] S. Tekin-Özan, and M. Barlas, Concentration of heavymetals in Ligula intestinalis L., 1758 plerocercoids(Cestoda) compared to its host’s (Tinca tinca L., 1758)organs from Beyşehir Lake (Turkey). Helminthol.45(2): 76-80, 2008.[16] B, Sures, Host-parasite interactions from anecotoxicological perspective. Parasitol. 47(3): 173-176,2001.[17] R. Poulin, Evolutionary ecology of parasites: Fromindividuals to community. Chapman and Hall Ltd:London, UK, 1998.[18] G.C. William, Natural selection: Domains, levels andchallenges. Oxford University Press: Oxford, UK, 1992.[19] S.N Luoma and P.S, Rainbow, Metal contamination inaquatic environment. Science and lateral management.Cambridge University Press, 2008.[20] L.R. Shugart, Molecular markers to toxic agents. In:Ecotoxicol.: A hierarchical treatment, (Eds.) Newman,M.C. and Jagoe, C.H. Lewis Publishers, Boca Raton:139, 1996.[21] S.M. Adams, Biomarker/bioindicator response profilesof organisms can help differentiate between sources ofanthropogenic stressors in aquatic ecosystems.Biomarkers, 6(1): 33-44, 2001.[22] N.R Verrengia-Guerrero, M.G. Taylor, N.A. Davies,M.A.M. P.A. Lawrence. K. Simkiss, and E.A. Wider,Evidence of differences in the biotransformation oforganic contaminants in three species of freshwaterinvertebrates. Environ. Pollut. 117: 523-530, 2002.[23] F Jirsa, M. Leodolter-Dvorak. and R. Krachler, Heavymetals in the nase, Chondrostoma nasus, L. 1758), andits intestinal parasite Caryophyllaeus laticeps, Pallas1781) from Austrian rivers, Bioindicative aspects.Archiv. Environ. Contamin. Toxicol. 55(4): 619-626,2008[24] J.H. Wanink, Prospects for the fishery on the smallpelagic Rastreneobola argentea in Lake Victoria.Hydrobiol. 407: 183-189, 1999.[25] J.A Neto, B.J Smith. and JJ. McAlister, Heavy metalconcentrations in surface sediments in a near-shoreenvironment, Jurujuba Sound, southeast Brazil.Environ. Pollut. 109: 1–9, 2000.5
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<strong>endoparasites</strong> <strong>in</strong> the natural water environment. Whenthe metal content <strong>in</strong> water with<strong>in</strong> the experimentalunits conta<strong>in</strong><strong>in</strong>g fish and parasites were <strong>in</strong>creased tenfoldthan metal concentration <strong>of</strong> the lake water <strong>in</strong> thelaboratory, all heavy metal concentrations <strong>in</strong> L.<strong><strong>in</strong>test<strong>in</strong>alis</strong> <strong>in</strong>creased between 10 to 35 time higherthan the concentration <strong>in</strong> tissues <strong>of</strong> its host. WhereasCu was demonstrated to be subject <strong>of</strong> elementcompetition between fish and parasite, Pb, Cd and Crdisplayed a partition<strong>in</strong>g <strong>in</strong> the fish host with parasiteshav<strong>in</strong>g higher concentration <strong>of</strong> these metals, whichwould render the <strong>Ligula</strong> <strong><strong>in</strong>test<strong>in</strong>alis</strong> <strong>in</strong> R. argenteahost a suitable as bio-monitor for exposure to thesemetals. It is evident that L. <strong><strong>in</strong>test<strong>in</strong>alis</strong> is sensitive<strong>in</strong>dicator and early warn<strong>in</strong>g sign for <strong>in</strong>creas<strong>in</strong>g Pb, Cdand Cr pollution. Given that the parasite is easy toidentify even <strong>in</strong> different host (Olson et al. 2000;Tek<strong>in</strong>-Özan and Kir Tek<strong>in</strong>-Örzan and Barlas 2008), itshigh abundance and high prevalence, it was found tobe suitable bio-monitor model for early warn<strong>in</strong>g signfor localized pollution by Pb, Cd and Cr <strong>in</strong> LakeVictoria.AcknowledgmentsThe authors would like to thank the RoyalNetherlands Embassy <strong>in</strong> collaboration with VictoriaInstitute for Research on Environment andDevelopment (VIRED) International for fund<strong>in</strong>g thisproject. The LVEMP Project also provided additionalsupport to which we are grateful. The authors thankMr. Lewela <strong>of</strong> Moi University, Biochemical Analysislaboratory for the <strong>in</strong>valuable assistance <strong>in</strong> samplecollection and analysis <strong>of</strong> heavy metals.References[1] B. Sures, Accumulation <strong>of</strong> heavy metals by <strong>in</strong>test<strong>in</strong>alhelm<strong>in</strong>ths <strong>in</strong> fish, facts, appraisal and perspectives.Parasitol. 126: 53-60, 2003.[2] B. Sures, Environmental parasitology: relevancy <strong>of</strong>parasites <strong>in</strong> monitor<strong>in</strong>g environmental pollution. Trends<strong>in</strong> Parasitol. 20(4): 170-177, 2004.[3] B. Sures, H. Taraschewski, and E. Jackwerth, Leadaccumulation <strong>in</strong> Pomphorhyncus laevis and its host. J.Parasitol. 80: 355-357, 1994a.[4] B. Sures, H. Taraschewski, and E. Jackwerth, Leadcontent <strong>of</strong> Paratenuisentis ambiguous (Acanthocephala),Anguillicola crassus (Nematodes) and their hostsAnguilla anguilla. Dis. Aquat. Org. 19: 105-107, 1994b.[5] B. Sures, H. Taraschewski. and E. Jackwerth,Comparative study <strong>of</strong> lead accumulation <strong>in</strong> differentorgans <strong>of</strong> perch (Perca fluviatilis) and its <strong>in</strong>test<strong>in</strong>alparasite Acanthocephalus lucii. Bull. Environ. Contam.Toxicol. 52: 269-273, 1994c.[6] B. Sures and H. Taraschewski, Cadmium concentration<strong>in</strong> two adult acanthocephalans, Pomphorynchus laevisand Acanthocephalus lucii, as compared with their fishhosts and cadmium levels <strong>in</strong> larvae <strong>of</strong> A. lucii ascompared with their crustacean host. Parasitol. Res. 81:494-497, 1995.[7] B. Sures, R. Siddall. and H. Taraschewski, Parasites asaccumulation <strong>in</strong>dicators <strong>of</strong> metal pollution. Internat. J.Parasitol. 33: 65-70. 1999.[8] J. Dvoracek, F. Tenora, V. Barus, and S. Kracmar,Concentrations <strong>of</strong> some heavy metals <strong>in</strong> <strong>Ligula</strong><strong><strong>in</strong>test<strong>in</strong>alis</strong> plerocercoids (Cestoda) and Philometraovata (Nematoda) compared to some their hosts(Osteichthyes). Helm<strong>in</strong>thol. 37(1):15-18, 2000.[9] B. Sures, The use <strong>of</strong> fish parasites as bio<strong>in</strong>dicators <strong>of</strong>heavy metals <strong>in</strong> aquatic ecosystems, a review. Aquat.Ecol. 35: 245-255, 2001.[10] C. Schludermann, S. Konecyny, S. Laimgruber, J.W.Lewis, F. Schiemer, A. Chovanec. and B. Sures, Fishmacroparasites as <strong>in</strong>dicator <strong>of</strong> heavy metal pollution <strong>in</strong>river sites <strong>in</strong> Austria. Parasitol. 126: 61-69, 2003[11] B. Sures and N. Reimann, Analysis <strong>of</strong> the trace metals<strong>in</strong> the Antactic host-parasite system Nototheniacoriiceps and Aspersentis megarhynchus(Acanthocephala) caught at K<strong>in</strong>g George Island, SouthShetland Islands. Polar Biol. 26: 680-686, 2003.[12] F. Thielen, S. Zimmermann, F. Baska, H. Taraschewski,and B. Sures, The <strong>in</strong>test<strong>in</strong>al parasite Pomphorhyncuslaevis (Acanthocephala) from barbel as bio<strong>in</strong>dicator formetal pollution <strong>in</strong> the Danube River near Budapest,Hungary. Environ. Pollut. 129: 420-429, 2004.[13] B. Sures, Host-parasite <strong>in</strong>teractions from anecotoxicological perspective. Parasitol. 47(3): 173-176,2007.[14] S. Tek<strong>in</strong>-Özan and I. Kir, Comparative study on theaccumulation <strong>of</strong> heavy metals <strong>in</strong> different 291 organs<strong>of</strong> tench (T<strong>in</strong>ca t<strong>in</strong>ca L. 1758) and plerocercoids <strong>of</strong> itsendoparasite <strong>Ligula</strong> <strong><strong>in</strong>test<strong>in</strong>alis</strong>. Parasitol. Res. 97:156-69, 2005.[15] S. Tek<strong>in</strong>-Özan, and M. Barlas, Concentration <strong>of</strong> heavymetals <strong>in</strong> <strong>Ligula</strong> <strong><strong>in</strong>test<strong>in</strong>alis</strong> L., 1758 plerocercoids(Cestoda) compared to its host’s (T<strong>in</strong>ca t<strong>in</strong>ca L., 1758)organs from Beyşehir Lake (Turkey). Helm<strong>in</strong>thol.45(2): 76-80, 2008.[16] B, Sures, Host-parasite <strong>in</strong>teractions from anecotoxicological perspective. Parasitol. 47(3): 173-176,2001.[17] R. Poul<strong>in</strong>, Evolutionary ecology <strong>of</strong> parasites: From<strong>in</strong>dividuals to community. Chapman and Hall Ltd:London, UK, 1998.[18] G.C. William, Natural selection: Doma<strong>in</strong>s, levels andchallenges. Oxford University Press: Oxford, UK, 1992.[19] S.N Luoma and P.S, Ra<strong>in</strong>bow, Metal contam<strong>in</strong>ation <strong>in</strong>aquatic environment. Science and lateral management.Cambridge University Press, 2008.[20] L.R. Shugart, Molecular markers to toxic agents. In:Ecotoxicol.: A hierarchical treatment, (Eds.) Newman,M.C. and Jagoe, C.H. Lewis Publishers, Boca Raton:139, 1996.[21] S.M. Adams, Biomarker/bio<strong>in</strong>dicator response pr<strong>of</strong>iles<strong>of</strong> organisms can help differentiate between sources <strong>of</strong>anthropogenic stressors <strong>in</strong> aquatic ecosystems.Biomarkers, 6(1): 33-44, 2001.[22] N.R Verrengia-Guerrero, M.G. Taylor, N.A. Davies,M.A.M. P.A. Lawrence. K. Simkiss, and E.A. Wider,Evidence <strong>of</strong> differences <strong>in</strong> the biotransformation <strong>of</strong>organic contam<strong>in</strong>ants <strong>in</strong> three species <strong>of</strong> freshwater<strong>in</strong>vertebrates. Environ. Pollut. 117: 523-530, 2002.[23] F Jirsa, M. Leodolter-Dvorak. and R. Krachler, Heavymetals <strong>in</strong> the nase, Chondrostoma nasus, L. 1758), andits <strong>in</strong>test<strong>in</strong>al parasite Caryophyllaeus laticeps, Pallas1781) from Austrian rivers, Bio<strong>in</strong>dicative aspects.Archiv. Environ. Contam<strong>in</strong>. Toxicol. 55(4): 619-626,2008[24] J.H. Wan<strong>in</strong>k, Prospects for the fishery on the smallpelagic Rastreneobola argentea <strong>in</strong> Lake Victoria.Hydrobiol. 407: 183-189, 1999.[25] J.A Neto, B.J Smith. and JJ. McAlister, Heavy metalconcentrations <strong>in</strong> surface sediments <strong>in</strong> a near-shoreenvironment, Jurujuba Sound, southeast Brazil.Environ. Pollut. 109: 1–9, 2000.5
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