Use of endoparasites, Ligula intestinalis plerercoid in ...

Use of endoparasites, Ligula intestinalis plerercoid in Rastreneobola argentea tobiomonitor increasing metal contamination in waters of Lake VictoriaElijah Oyoo-Okoth 1* ., Leah Cherop 1 , Victoria Chepkirui-Boit 1 , Odipo Osano 2 , Veronica Ngure 31 Department of Fisheries and Aquatic Sciences, Moi University, Eldoret, Kenya, P.O. Box 1125, Eldoret - Kenya.2 School of Environmental Studies, Moi University, P.O. Box 3900, Eldoret.3 Department of Wildlife Management, Moi University, Eldoret, Kenya, P.O. Box 1125, Eldoret - Kenya.* Corresponding author Tel No: +254720222082 Email: elijaoyoo@yahoo.comAbstract: The ability of endoparasites to detecteven lowest metal concentration due to their enormousaccumulation capacity has made them suitable waterpollution biomonitors than their fish hosts. This studyevaluated the metal accumulation ability of Ligulaintestinalis in its intermediate cyprinid host silversardine (Rastreneobola argentea) from Lake Victoriain the natural environment and in laboratory conditionas a possible sentinel tool to biomonitor five metals.Metal concentration in fish and parasites exhibitedsite-specific variations relative to the anthropogenicactivities along the coastal zone of Lake Victoria. Thefish bioaccumulated lead (Pb), cadmium (Cd),chromium (Cr), and copper (Cu) by factor 5.2, 4.2, 6.4and 3.5 respectively than its host under normalenvironmental conditions of the lake. When the metalcontent in water within the experimental unitscontaining fish and parasites were increased ten-foldthan 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. This studysupports a recommendation of incorporating thecestode endoparasite (L. intestinalis) in a cyprinid host(R. argentea) as suitable early warning bio-indicatorof heavy metal pollution and should thus be useful totrack increasing localized heavy metal pollution.Keywords: Biomonitor, Heavy metals, Lake Victoria,Ligula intestinalis, Rastreneobola argentea.1. IntroductionParasites are an essential part of the aquaticenvironment and represent a significant proportion ofaquatic biomass. The relationship betweenenvironmental pollution and parasitism in aquaticorganisms and the potential role of endoparasites aswater quality indicators have received increasingattention during the past two decades (Sures, 2003;Sures, 2004). Since parasites are sensitive toenvironmental change, others are more resistant thantheir hosts and tend to increase in numbers in pollutedconditions (Sures, 2004); they are now regarded as auseful indicator of aquatic health.Fish, parasite and metal interactions havegenerated large pool of literature from environmentalpollution monitoring perspective (Sures et al.1994a,b,c; Sures and Taraschewski, 1995; Sures et al.,1999; Dvovareck et al. 2000; Sures, 2001; Sures,2003; Schludermann et al., 2003; Sures and Reimann,2003; Thielen, et al., 2004; Tekin-Ộzan and Kir, 2005;Tekin-Ộzan and Barlas, 2008). A major conclusionfrom these literature revealed that for different host–parasite associations, intestinal parasites accumulate anumber of metals to concentrations several hundredtimes higher than the levels in host tissues (Sures,2001, 2003, 2004; Thielen, et al., 2004) thus renderparasites sensitive metal accumulation biomonitorsthan their fish host. Recently Sures (2007) indicatedthat parasites can also act as metal sinks for its fishhost. It is apparent that any changes to metalconcentration in the fish tissues are likely to altermetal bioavailability and toxicity.One important question in the host-parasiteevolutionary ecology (Poulin, 1998) is whetherparasite-host induced modification observed in bothnatural and experimental conditions is adaptive orsimply coincident (Williams, 1992). Whendetermining the bio-availability and toxicity of metalsto fish in presence of endoparasites, the resultsobtained are variable and studies conducted in thefield often differ with those in the laboratory (Luomaand Rainbow, 2008). Organisms under natural fieldconditions may respond quite differently to pollutantexposures, under laboratory conditions (Shugart,1996). Laboratory studies generally lack ecologicalrealism, because of many environmental factors thatcan influence organism responses at all levels ofbiological organisation (Adams, 2001). According toVerrengia-Guerrero et al. (2002), the extent oforganism responses depends on the toxico-kinetic andtoxico-dynamic processes that occur once a metaltoxicant has entered the organism. Nonetheless, thereare very few field and laboratory studies on the metalconcentration in fish and its parasites.Currently, cestodes affect large number of fishspecies and can survive in wide and highly variableenvironments (Jirsa et al. 2008). Further studies onsystematically different parasites from differentmicrohabitats in fish as well as from differentenvironments are required for cestode-fish hostgrouping as a way to further the development ofbiomonitoring tools for metal contamination in theaquatic environments. For this, the aim of this studywas to evaluate the metal accumulation ability of acestode (L. intestinalis) in a cyprinid fish host (R.argentea) as a possible sentinel host-parasite1

association in monitoring increasing heavy metalpollution in lacusterine environment. This hostparasiteassemblage was analyzed at different sites toidentify the variable metal exposure in the coastalzone of Lake Victoria.2. Materials and methods2.1 Study area and sampling sitesLake Victoria, the second largest freshwater bodyin the world (area 68,800 km 2 ), is generally shallow(mean depth 40 m) and lies in a catchment of about184,000 km 2 , shared by three riparian states (Kenya,Tanzania and Uganda). Site selection in Kenya wasbased on the anthropogenic activity profiles along thecoastal zones (Fig. 1). Site 1 (Kisumu City) has apopulation of about 1.1 Million and is a centre ofurban development with various industries anddrainage of intense agriculture. Site 2 (Kendu-Bay) isa rural agricultural area without fertilizer inputs. Site 3(Karungu) receives drainage from small gold mines.Site 4 (Port Victoria) is a rural area, receiving waterfrom the River Nzoia, containing effluents from twosugar factories and a paper mill factory situated about100-150 km upstream from the Lake.L. intestinalis involves three hosts, a crustacean(copepod), a fish (e.g. R. argentea) and a bird (e.g.pied Kingfisher or Cormorant). Copepods carryinfective stages of the parasite, which are transferredto the fish R. argentea and subsequently to the fishconsumers in the coastal zone of the Lake Victoria.Accumulated metals are thus transferred via the samefood chain.Fish samples were obtained from local fishermenon two sampling occasions in June 2006 from the sitesS1, S2, S3 and S4 using a beam trawl with 5 mmstretched mesh; fish was attracted in the night bylamps. The catch data are presented in Table 1. Tominimize contamination, all materials used in theexperiment were previously washed in ultra purewater. Fish were weighed (to the nearest 0.1 g),measured (folk length in mm) and dissected.Dissection of the fish was done on the shore usingstainless steel instrument pre-cleaned in doubledistilled water. In parasitized fish, parasites wereremoved using stainless steal instruments, counted,weighed and stored in glass vials and later transferredto Teflon vials and freeze dried, awaiting furtheranalysis. Both parasitized and unparasitized fish werebagged and frozen until processed in the laboratoryusing metal-free techniques in the Netherlands.2.3 Metal enrichmentsWater from Lake Victoria was enriched using Pb,Cd, Cr and Cu. The concentration of the specific metalapplied were 10 times the initial concentration of theLake water in site 1. The parasitized and nonparasitized fish were then transferred to the water andleft in the solution for 96 h.Fig. 1. Map of Lake Victoria basin (Kenya) showing thesampling sites2.2 Fish and endoparasite collectionThe fish host chosen in this study was a cyprinid, R.argentea (Pellegrin, 1904). This fish occurs in a highabundance in Lake Victoria, more than any otherspecies. During the past eight years it has composedbetween 37 – 45% of the commercial fish catch(Wanink, 1999). Due to its relatively low price, itdominates as a source of protein among the poor lakeshore communities, mainly because other larger fishspecies are preferred for trade, including export for thecountry’s foreign exchange earning. The life cycle of2.4 Metal analysisThe frozen samples were thawed, crushed andhomogenized using a Fritsch, Pulverisette 5, planetarymill (Fritsch GmbH Laborgerate, Idar-Oberstein,Germany) for 5 minutes at 400 rpm. About 0.5 g ofsample were accurately weighed in Telflon (© polytetra-fluor-etheen(PTFE), DuPont) high pressurevessels. Then 4.0 ml concentrated nitric acid (65%),1.0 ml concentrated hydrochloric acid (37%) and 1.0ml ultra pure water was added to the samples. Sixsamples were placed in the carousel of a PaarMicrowave oven (Anton Paar GmbH – Graz –Austria).Digestion took place at 200°C and 70 bar pressureduring 15 minutes. After cooling the obtained clearsolutions were quantitatively poured in 50mlvolumetric flasks and diluted to the mark with ultrapure demineralized water. Finally the diluted solutionswere transferred into acid cleaned polyethylene bottles.All elements were determined by means of inductivelycoupled plasma-optical emission spectrometry (PerkinElmer Optima 3000 XL, ICP-OES) using the PEcalibration standards. The concentrations werecalculated as mg kg -1 dry weight. The quality of theanalytical process was controlled by the analysis ofIAEA MA-A-3/TM certified standard referencematerial of shrimp. Measured values deviated lessthan 10% from the certified values.2

2.5 Statistical analysesMetal concentrations in the biota were statisticallyanalysed using a one-way ANOVA. Post-Hoc HSDwas used for Post-hoc discrimination between themeans. Relationships between metal concentrations inthe parasite and the fish were analyzed using linearregression analysis.3. Results and discussionThe concentration of the four heavy metal (Pb, Cd,Cr and Cu) in water at the four sampling sitespreviously selected is shown in Tab. 1. Though thevariation in concentration among the sites was slight,the concentration of all metals displayed significantdifferences among sampling sites (P < 0.05).Sampling site 1, had higher levels of Pb, Cd and Cuthan other sites. However, the concentration of Cr wasfound to be elevated in site 3 when compared to othersites. This show evidence of anthropogenic influenceon heavy metal concentration, which resulted indifferential spatial heavy metal distribution. Currentresults indicate low levels of heavy metal whencompared to most countries (Neto et al. 2000; Fatokiand Mathabatha 2001; Ruiz 2001; Adamo et al. 2005;Chen et al. 2006) but signs of increasing heavy metalis evidence when compared to earlier studies in thisarea (Wandiga 1981; Wandiga et al. 1983; Onyari andWandiga 1989; Mwamburi and Oloo, 1997).Tab. 1 Concentration of the measured metals in water atthe sampling sitesHeavymetalsSampling sitesS1 S2 S3 S4Pb 1.0 ± 0.1 c 0.3 ± 0.05 b 0.3 ± 0.03 b 0.3 ± 0.02 aSince the variation in metallic concentrationswithin the aquatic organisms reflects the net effect ofcompeting processes, encompassing uptake anddepuration, bioaccumulation under describes the netaccumulation of a chemical into the tissue of anorganism as a result of uptake from all environmentalsources (Burkhardt et al., 2003). Under normal waterenvironment, the uptakes of heavy metals are usuallymasked when the total heavy metal in water is low.The concentration of heavy metals in fish tissues andin the parasites in ambient water environment isshown in Fig. 2. Metal concentration in all the fishsamples displayed significant spatial variations as didthe specific metal contents in the fish parasites (P 0.05).The measured concentration of heavy metals inwater after enrichment are shown in Tab. 2, whichreflect the total heavy metal content to be taken up bythe organism from the aquatic environment.Tab. 2 Measured heavy metal in enriched watermedia (from site 1)Heavy metalsHeavy metal concentrationPb 9.20 ± 0.74Cd 0.92 ± 0.22Cr 3.54 ± 0.42Cu 7.82 ± 0.32Metal concentrations mg kg -1 dw)40.0 Pb1.5 Cd32.024.016.08.00.05.04.03.02.01.00.0FishParasiteFishCrParasiteFishParasiteSampling sitesFig. 2. Heavy metal concentrations in fish and fishparasites (mg kg -1 dw) at the four sampling sites in LakeVictoriaFish1 2 3 4Parasite1.20.90.60.30.015.012.09.06.03.00.0FishParasiteFishParasiteCuFishParasiteFish1 2 3 4Parasite3

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. 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