COPYRIGHT AND CITATION CONSIDERATIONS FOR THIS THESIS/ DISSERTATION Attribution — You must give appropriate credit, provide a link to the license, and indicate if o changes were made. You may do so in any reasonable manner, but not in any way that suggests the licensor endorses you or your use. NonCommercial — You may not use the material for commercial purposes. o ShareAlike — If you remix, transform, or build upon the material, you must distribute your o contributions under the same license as the original. How to cite this thesis Surname, Initial(s). (2012) Title of the thesis or dissertation. PhD. (Chemistry)/ M.Sc. (Physics)/ M.A. (Philosophy)/M.Com. (Finance) etc. [Unpublished]: University of Johannesburg. Retrieved from: https://ujdigispace.uj.ac.za (Accessed: Date). Bio-accumulation of selected metals in the organs and tissues of the redknobbed coot, Fulica cristata, reed cormorant, Phalacrocorax africanus and sacred ibis, Threskiornis aethiopicus, in mine and industrial polluted freshwater ecosystems. By PIETER HERMANUS VAN EEDEN· Thesis presented in fulfilment ofthe requirements for the degree PHILOSOPHIAE DOCTOR . In ZOOLOGY in the FACULTY OF NATURAL SCIENCES at the RAND AFRIKAANS UNIVERSITY SUPERVISOR: Prof. H.J. Schoonbee CO-SUPERVISOR: Prof. H.H. du Preez NOVEMBER 1994 SUMMARY The present study deals withthe effects ofmetal-polluted aquatic habitats at five different localities on the Witwatersrand and the Orange Free State on the concentrations oflead, nickel, copper and cadmium in the organs and tissues of the Redknobbed Coot, Fulica cristata, the Sacred Ibis, Threskiomisaethiopicus, andthe Reed Cormorant,Phalacrocoraxafricanus. The physical and chemical conditions of the water and the sediments which prevailed during the period of survey at the various sampling sites suggest that concentrations of parameters such as phosphates, nickel and lead in a number ofcases exceeded the limitslaid down by Kempster et at. (1980) for acceptable river water quality standards in South Africa. The major sources ofpollution responsible for these conditions can primarily be related to sewage, mine and industrial effiuents (urban) as well as agricultural practices (rural), respectively. Mining activities were largely responsible for the acidification and miniralization as well as metal pollution of the water and sediments, especially so at the Marievale Bird Sanctuary in the Blesbokspruit catchment area. However, automobiles are suspected to contribute much towards the lead concentrations in the water andsedimentsat allthe samplingsites. Levels ofcadmiumwere generallylow and maybe the onlyone ofthe four metals analysed which truly reflected unpolluted, environmentalconditions for thismetal inthe water and sedimentsofallthe samplingsites. The nutrient loads which suggest mild to moderate eutrophication of the water at all the localities can largely be attributed to sewage effiuentsand surface runoffwaters from the surrounding townships on the Witwatersrand as well as from inorganicfertilizers from farm lands inthe vicinityofthe Steynsrus and Senekalfarm dams in the Orange Free State. These conditions resulted in the overall increase in primary and secondary production of the affected waters which also coincided with the development of submerged and floating water weeds such as Potamogeton pectinatus and Azolla filliculoides, respectively. The herbivorous Redknobbed Coot and to a lesser extent the piscivorous Reed Cormorant, benefitted directlyor indirectlyfrom these conditions. Data obtained duringthe investigationpresent a complex situation in terms ofthe environment and thebiologicalavailabilityofthe four metalsunder discussion. Anumber offactors inboth the abiotic and biotic components may have had an effect on fluctuations in metal concentrations. These may have acted individually and/or synergistically, making the interpretation of the data difficult. Cadmiumoccurred inthe lowest concentrations ofall four metals in all four the organs and tissues during allfour seasonsofinvestigation.In the case ofthe rest ofthe metals as wellas the organs and tissues no specific, clear seasonal trend or sequence in the concentrations of the metals was discernible. Copper in the kidney and liver and lead in the bone and blood tissues had the highest mean concentrations over the four seasons of investigation. As far as the winter and summer seasonaltendencies are concerned, statisticallysignificantdifferencesoccurred in the concentrations ofsome metalsin specificorgans and tissues between the winter and summer seasons, respectively. However, values recorded were not necessarily higher during a particular season. Lead (liver) and cadmium (kidney) concentrations were found to be significantly higher in winter 1991 whilst cadmiumand copper (both inthe blood) were significantly lower duringthis same season, compared to winter 1992. Concentrations ofnickeldid not differsignificantly between organs and tissues such as the liverand blood for particular seasons. It was only nickel in the kidney and cadmium in the bonetissuewhichreflecteddefiniteseasonaltrends for the four successiveseasons ofinvestigation. The Germiston lake sediments contained relatively high concentrations of metals such as nickel (industrial pollution) and lead (mainlyfrom street surface runoff which enters the lake via storm water drains). Recently, anaccidental spillofcadmium-containing effiuentinto the lake occurred via a stormwater drain along the south-eastern perimeter of the lake (Schoonbee, personal 11 communication). It is therefore not surprising that the liver and kidney, but not the bone tissue of coot caught at this locality contained the highest concentrations ofthis metal. The absence ofmetal processing industriesinthe catchment ofthe Florida lake and ofthe Steynsrus farm dams reflect the low liver and kidney concentrations of cadmium, nickel and copper, respectively. The highest concentrations of nickel, cadmium, copper and lead (Natalspruit wetland) in the blood ofthe coot may be related to its dietary preferences which include P. pectinatus, A. filliculoides and Lemna sp. These aquatic weeds are known to beefficient bio-accumulators ofmetals from metal-polluted aquatic environments. The statistical evaluation ofthe data point towards geographical differences in the concentrations ofthe metals inthe organs and tissues ofthe coot from the five different localities. However, in terms ofactual metal concentrations recorded, significant differences existed between coots ofthe reference site (Steynsrus farm dams) and those from the other four localities (East Rand). It can be accepted that the dietary preferences ofthe herbivorous Redknobbed Coot, the omnivorous Sacred Ibis and the piscivorous Reed Cormorant as well as the metal content inthe food items all play an important role in the actual uptake and bio-accumulation of lead, nickel, copper and cadmium in the organs and tissue ofthese bird species. This particularly applies to birds collected from the Natalspruit wetlands known to be seriously polluted by effiuents from metal-processing industries and mines. In the case ofall three species the cadmium levels were consistently lowest in all four the organs and tissues. Highest concentrations of this metal occurred in the kidneys, especially inthe case ofthe Sacred Ibis andinterestinglyin the bone tissue ofthe Redknobbed Coot. The maximum blood cadmium concentrations were recorded for the Reed Cormorant. Copper, nickel and lead were found in much higher concentrations in the various organs and tissues than cadmium, with copper clearly being the dominant metal by weight in the liver ofall three species of birds. Nickel and lead occurred in the highest concentrations in the bone tissue ofall three species with concentrationsbeing as much as sixtimes higher than those ofcadmium or copper. Ofthe three species, the Reed Cormorants generally exhibited the highest bone lead concentrations. Nickel and lead values for the blood and kidneys were approximately 1-3 times higher than the concentrations of those metals inthe bone tissues. With the exception ofthe liver, significant differences were recorded for cadmium in all the other organs and tissues among the three species. In the case ofthe other metals, significantdifferences were recorded betweenat least two ofthe three species. The three bird species under investigation have distinctive different dietary habits with all three species feeding actively on metal-polluted food items at the localities where they were collected from. It can therefore be assumed that the metal concentrations found in their tissues and organs must largely originate from these food items. Metal concentrations in the Kikuyu grass Pennisetum clandestinum which is actively eaten by the coot, vary considerably in its metal contents from one locality to another and also during the different seasons of the year. The Sago Pondweed P. pectinatus as well as the Red Water Fern A. filliculoides, which are favoured by the Redknobbed Coot, are both knownto accumulate substantial quantities ofmetals from the sediments and water of metal-polluted habitats. A similar picture evolved when looking at dietary habits and the possible uptake ofmetals from theirfood bythe Sacred Ibis (scavengers) andtheReed Cormorant (predator), respectively. The ibis obtain its food and consequently its metal loads from a variety offood items in the areas where this bird occurs whilst the Reed Cormorant may obtain metal loads by feeding on fishand largemacro-invertebrates from these metal-polluted waterbodies. It is clear from the results ofthe present investigation that the water and sediment concentrations of lead, copper and nickel in most ofthe different localities were usually higher than the recommended water quality guideline values while cadmium was well within the set limits for the protection of aquatic life.It is also apparent that the coots from the five geographically different populations as III well asthe Sacred Ibisand ReedCormorant from theNatalspruit wetlands were clearly ableto bio accumulateallfourmetals. Bottom sediments may play a very important role in the retention and distribution of cadmium, copper, nickel and lead in the various aquatic environments. They act as reservoirs for metals, releasingandadsorbingmetalsto and fromthe water columnthrough various processes. The results indicated that the Redknobbed Coot, Sacred Ibis and Reed Cormorant were all three exposed to chronicallyhigh levelsofnickel, lead, copperand cadmiumfor prolonged periods oftime. Emerging from this investigation is a picture which suggests that the levels of copper, cadmium, nickel andlead inthetissues andorgans ofthe Redknobbed Coot, Sacred Ibis and Reed Cormorant reflectthenatureoftheir dietaryintake ratherthan the specificgeographicaland/or seasonalpatterns ofmetal accumulation. It mustbe borne in mind that, besides the concentrations of metals in the abiotic environment and in the diet of these particular bird species, various other factors can contribute to the observed geographical variations in metal concentrations recorded during this investigation. The metal-polluted streams, lakes and wetlands on the Witwatersrand and even elsewherein SouthAfrica,canserve asidealfield laboratoriesinassessingthis specificsituation. IV QpSOMMING Die huidige ondersoek handel oor die effek van metaalbesoedelde akwatiese habitatte by vyf verskillende lokaliteite aandie Witwatersrand en die Oranje Vrystaat op die konsentrasies van lood, nikkel, koper en kadmium in die organe en weefsels van die Bleshoender Fulica cristata, die Skoorsteenveer Threskiornis aethiopicus en dieRietduikerPhalaeroeorax africanus. Die heersende fisiese en chemiese toestande van die water en sedimente gedurende die opnameperiode soos aangetrefby dieverskillende lokalitiete, dui daarop dat die konsentrasies van parameters soos fosfate, nikkel en lood in 'n hele aantal gevalle die perke soos neergele deur Kempster et al. (1980) vir aanvaarbare rivierwater- kwaliteitstandaarde oorskrei het. Die belangrikste bronne van besoedeling verantwoordelik vir hierdie toestande, kan hoofsaaklik toegeskryfword aan riool-, rnyn- en industriele afloopwaters (stedelik) sowel as landbougebruike (landelik), onderskeidelik. Mynbouaktiwiteite is grootliks verantwoordelik vir die versuring en mineralisering sowel as metaalbesoedeling van die water en sedimente. Dit geld veral vir die Marievale Voelreservaat in die Blesbokspruitopvanggebied. Dit word egter vermoed dat motorvoertuie heelwatbydratot dieloodkonsentrasie indiewaterendie sedimente soos gevind by al die lokaliteite. Vlakke van kadmium was oor die algemeen laag en is dit die enigste van die vier metale wat algerneen onbesoedelde toestande vir hierdie element in die water en sedimente verteenwoordig. Die nutrientladingswat dui op ligte tot matige eutrofikasie van die wateromgewing by al die lokaliteite kan grootliks toegeskryf word aan rioolafloop- en stormwaters vanaf die omliggende stedelike gebiede aan die Witwatersrand asook van organiese kunsmisstowwe vanaf landeryein dieomgewingvan die damrneby Steynsrus enSenekal. Hierdie toestande het geleitot die algemene toename in die primere en sekondere produktiwiteit van die geaffekteerde waters wat terselfdertyd saarngeval het met die oormatige ontwikkeling van onderwater- en drywende waterplante soosPotamogetonpeetinatus enAzollafilliculoides, onderskeidelik. Die plantvretende Bleshoender en tot 'n mindere mate die predatoriese Rietduiker het direk of indirek by hierdie toestande gebaat. Dataverkrygedurendedieondersoekbied 'n komplekse toestand interme van die omgewing en die biologiese beskikbaarheidvan die vierrnetale onder bespreking aan.'n Aantal faktore rakende beide die biotiese en abiotiese kornponente kon 'n effek gehad het op die skommelinge gevind in metaalkonsentrasies. Hierdie faktore kon individueel en/of sinergisties opgetree het, wat die vertolking vandie data uiters bemoeilik het. Kadmium het voorgekom in die laagste konsentrasies vanalvier metale in dievierorgane enweefsels van die drie voelsoorte. In diegeval van die res van diemetale sowel as die organe en weefsels isgeen spesifieke, duidelikeseisoenstendense ofvolgorde in die konsentrasies van die rnetale waargeneem nie. Koper in die nier en lewer en lood in die beenweefselsenbloed hetdie hoogste gemiddelde konsentrasies oor die vier seisoene van ondersoek opgelewer. In soverre dit die winter- en somerseisoenstendense betref, is statisties-beduidende verskille gevind in die konsentrasies van sommige metale en weefsels tussen die winter- en somerseisoene, onderskeidelik. Waardes aangetref was nie noodwendig hoer gedurende bepaalde seisoene nie. Lood- (Iewer) en kadmium- (nier) konsentrasies is gevind om betekenisvol hoer gedurende die winter van 1991 te wees terwyl kadmium en koper (beide in die bloed) weer betekenisvol laer gedurende dieselfde seisoen was vergeleke met die winter van 1992 was. Konsentrasies van nikkel hetniebetekenisvol verskil tussenorgane enweefsels soos dit weIdie geval wasvir die leweren bloedtydens bepaalde seisoene nie.Dit was slegsnikkel indie nier en kadmium in die beenweefsel wat definitiewe seisoenstendense weerspieel het vir die vier opeenvolgende seisoenevan ondersoek. v Die Germistonmeer sedimente bevat relatief hoe konsentrasies van metale soos nikkel (nywerheidsbesoedeling) en lood (hoofsaaklik van stormwaters wat die meer op verskeie plekke bereik). Onlangs was daar 'ntoevallige stortingvan kadmiumbevattende afloopwatersin die meer via 'n stormwaterkanaal aan die suid-oostelike oewer van die meer (Schoonbee, persoonlike mededeling). Dit is dus nie verbasend dat die lewer en nier, maar nie die beenweefsel van die Bleshoenderwat by hierdie lokaliteit versamel is, die hoogste konsentrasies van hierdie metaal vir al die lokaliteite opgelewer het nie. Die afwesigheid van metaalverwerkingsnywerhede in die opvanggebied van die Floridameer en in die omgewing van die Steynsrus plaasdamme word weerspieel deur die lae lewer- en nierkonsentrasies van kadmium, nikkel en koper, onderskeidelik. Die hoogste konsentrasies van nikkel, kadmium, koper en lood (Natalspruit vleiland) in die bloed van die Bleshoender mag "n verband hou met sy voedselvoorkeure wat P. peetinatus, A. fillieuloides en Lemna sp. insluit. Hierdie akwatiese makrofiete is bekend vanwe hulle doeltreffende bio akkumulering van metale in metaalbesoedelde wateromgewings. Die statistiese evaluering van die data duiop geografieseverskille in die konsentrasiesvan die metale in die organe enweefsels van die Bleshoendervir dievyfverskillende lokaliteite. Interme van diewerklike metaalkonsentrasies gevind kom daar egter betekenisvolle verskille voor tussen die Bleshoenderbevolkings van die kontrole lokaliteit (Steynsrus plaasdamme) en dievan die andervier lokaliteite (Oos-Rand). Dit kan aanvaar word dat die dieetsvoorkeure van die plantvretende Bleshoender, die omnivore Skoorsteenveer en die visvretende Rietduiker sowel as die onderskeie metaalinhoude van die voedselitems, gesamentlik 'n belangrike rol speel in die werklike opname in bio-akkumulering van die vier metale in die organe en weefsels van hierdie voelsoorte. Dit geld veral vir voels wat in die Natalspruit vleilande voorkom wat bekend is vir die emstige besoedeling van afloopwaters vanaf metaal-verwerkingsindustriee en myne. In die geval van al drie spesies was die kadmiumvlakke deurgaans die laagste in al vier die organe en weefsels. Hoogste konsentrasie vir hierdie metaal het voorgekom in die niere, veral in die geval van die Skoorsteenveer en interessant genoeg, in die beenweefsel van die Bleshoender. Die maksimum bloedkadmiumkonsentrasies is gevind vir die Rietduiker. Koper, nikkel en lood is inveel hoer konsentrasies in die verskillende organe en weefsels aangetrefas wat dit die geval was vir kadmium met koper duidelik die dominante metaal per massa in die lewer van al drie voelsoorte. Nikkel en lood kom in die hoogste konsentrasies in die beenweefsel van al drie voelsoorte voor met waardes wat tot ses keer hoer was as die vir kadmium of koper. Van die drie voelsoorte vertoon die Rietduiker oor die algemeen die hoogste beenloodkonsentrasies. Nikkel- en loodwaardes vir diebloed en niere was ongeveer een tot drie keer hoer as die konsentrasies hiervan in die beenweefseI. Met die uitsondering van die lewer, is betekenisvolle verskille gevind vir kadmium in al die ander organe en weefsels tussen die drie voelsoorte. In die geval van die ander metale is beduidende verskille gevind tussen minstens twee van die drievoelsoorte, Die drie spesies van voels wat ondersoek is vertoon opvallende dieetsverskille maar met aldrie wat aktiefvoed metaalbesoedelde voedselitemsby die onderskeie lokaliteite waar hulle aangetrefword. Dit kan dus aanvaar word dat die metaalkonsentrasies in hulle weefsels en organe grootliks verband moes hou met hierdie betrokke voedselitems. Metaalkonsentrasies in die Kikuyugras Pennisetum clandestinum wat aktief benut word as voedsel deur die Bleshoender, wissel aansienlik van een lokaliteit na die ander en ook tussen die verskillende seisoene van die jaar. Die watergras P. pectinatus sowel as die Rooiwatervaring A. filliculoides wat voorkeurvoedsel is vir die Bleshoender, is beide bekend daarvoor vir hul vermoeens om aansienlike hoeveelhede van metale vanuit die sedimente en waterkolom van metaalbesoedelde wateromgewings te akkumuleer. 'n Soortgelyke patroon word gevind wanneer daar gekyk word na die voedingsgewoontes en die moontlike opname van metale vanuit hulle voedsel,deur die Skoorsteenveer (aasdier) en die Rietduiker (predator), onderskeidelik. Die Skoorsteenveer verkry sy voedsel, en ook die metale VI vanaf'n verskeidenheid vanvoedselitems in die omgewings waar hierdie voel voorkom terwyl die Rietduiker metale opneem deur te voed op vis en groter makro-invertebraatorganismes van hierdie metaalbesoedelde wateromgewings. Uit die resultate verkry tydens die huidige ondersoek is dit duidelik dat die water- en sedimentkonsentrasies vir lood,koper ennikkel in diemeeste van die lokaliteite gewoonlik hoerwas as die aanbevole waterkwaliteitsriglyne vir die beskerming van akwatiese lewe terwyl kadmiumkonsentrasies in aldie gevalle binne hierdie standaarde voorgekom het. Dit is ook duidelik dat dieBleshoendervan alvyf geografies- verski1lende bevolkings sowel as die Skoorsteenveer en Rietduiker van die Natalspruitvleilande onteenseglik in staat was omal vier metale te bio akkumuleer. Bodemsedimente spee1 waarskynlik 'n belangrike rol in die retensie en verspreiding van kadmium, koper, nikkel en lood in die verskillende akwatiese omgewings. Dit kan optree as stoorplek vir metale en die vrystelling en adsorpsie van metale na en vanaf die waterkolom deur midde1 van verskeie prosesse. Die resultate toon aan dat die Bleshoender, die Skoorsteenveer en Rietduiker al drie blootgeste1 was aan chronies-hoe vlakke van nikkel, lood, koper en selfs ook kadmium vir langdurigetydperke. Voortvloeiend uit die huidigeondersoek kom 'n bee1d na yore wat daarop dui dat die vlakke van koper, kadmium,nikkel enlood in dieweefsels en organe van al drie voelsoorte 'n weerspieeling is van die tipes voedsel wat hulle ingeneem het, eerder as die spesifieke geografiese en/of seisoenspatrone van metaalakkumulering. Dit moet egter in gedagte gehou word dat naas die konsentrasies van metale in die abiotiese omgewing asook in die onderskeie diete van die betrokke voelsoorte, daarverskeie anderfaktore iswat kon bydratot diewaargenome geografiese variasiesin metaalkonsentrasies wat gevindis tydens hierdie ondersoek. Die metaalbesoedelde strome, mere en vleilande aan die Witwatersrand en selfs elders in Suid-Afrika, kan sonder twyfel dien as ideale veldlaboratoriaindieevalueringvan hierdiespesifiekesituasie. VII ACKNOWLEDGEMENTS I herebywishto expressmysincerest thanks to: • JesusChrist, myLord andSaviour, for providing me with the strenght and courage over the years ofstudy. • Prof H.I. Schoonbee forhis constant support, encouragement andmuch appreciated criticismand adviceduringthe course ofmy studies. • Prof H.H. duPreezfor hismany usefullcomments and advice duringthe writing ofmythesis. • Mywife Karen-Usefor her constant love, support and for the proofreading ofthe manuscript. • My parents, Mr. and Mrs. I.A. VanEeden, for their moraland financial assistance over the years duringmystudies at RandAfrikaansUniversity. • Louis and Louise de Wet,Louise Fleischer, AminaAdendorff, Veronica Steenkamp, Paul Grobler and Gerhard lanse van Rensburg for all their friendship, encouragement and help during the various fieldsurveys andlaboratoryanalysisofthe data over the years. • Juan Viljoen and Rene Bredenkamp as well as her parents for much appreciated assistence and accommodation during fieldcollections ofbirdsat Steynsrus. • DirkErIank forthe equipment andtransport provided for myfieldexcursions. • The teaching, technical and secretarial staff ofthe Department of Zoology for their respective assistance duringmy studies. • The Rand Afrikaans University for facilities and equipment provided which made this study possible. • The Water Research Commission and the City of Germiston for financial support which made thisstudy possible. • The Cities ofRoodepoort and Germiston for permission to collect material at the Florida and Germiston Lake areas. • DriesLouwaswell asHennie Basson Snr. andJnr. for their constant support and help during the periods ofcollection ofsamples atthe Vlakplaats WaterPollution Control Works. • The Transvaal and Orange Free State Provincial Administrations for permits granted for the collection ofthe various bird speciesinthese two provinces. • Marius de Jager from Wirsam Scientific Instruments for his much appreciated advice in the operation ofthe atomic absorption spectrometer. • Wynand Schoonbee for hismuch appreciated technical assistance during the computer processing ofthe manuscript. YI11 CONTENTS Chapter 1 Introduction 1 Chapter2 The avifauna ofmetal-pollutedwetlandsinthe Transvaalwith referenceto the selection ofbirds as bio-indicatorsofmetal pollution 12 Chapter 3 Description ofthe various sampling localities 27 Chapter4 Noteson the geographical distributionand general ecologyofthe Sacred Ibis, Redknobbed Coot and Reed Cormorant 34 Chapter 5 Materials and methods 44 Chapter6 The physico-chemical qualityand metal concentrations inthe water and sediment at the different samplinglocalities 56 Chapter7 Seasonal variations ofmetalconcentrations in selected organs and tissues ofthe Redknobbed Coot from ametal polluted wetland 76 Chapter8 Metal concentrations in selected organs and tissues offivegeographically distinct Redknobbed Coot populations 94 Chapter9 Comparative metalconcentrations inorgans and tissues ofthree species ofbirdsfrom a polluted wetland 112 Chapter 10 Metal concentrations in somefood itemsconsumed by the Redknobbed Coot, Reed Cormorant and Sacred Ibis 131 Chapter 11 General discussion 141 Chapter 12 Concluding remarks and recommendations 157 IX
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