The Incidence of Deformities in Chironomus spp. from Port Hope Harbour, Lake Ontario

The Incidence of Deformities in Chironomus spp. from Port Hope Harbour, Lake Ontario

J. Great Lakes Res. 13(1):88-92 Internat. Assoc. Great Lakes Res., 1987 NOTE THE INCIDENCE OF DEFORMITIES IN CHIRONOMUS SPP. FROM PORT HOPE HARBOUR, ...

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J. Great Lakes Res. 13(1):88-92 Internat. Assoc. Great Lakes Res., 1987

NOTE THE INCIDENCE OF DEFORMITIES IN CHIRONOMUS SPP. FROM PORT HOPE HARBOUR, LAKE ONTARIO

W. F. Warwick Department of the Environment National Hydrology Research Institute ]] Innovation Boulevard Saskatoon, Saskatchewan S7N 2X8 and

J. Fitchko, P. M. McKee, D. R. Hart, and A. J. Burt Beak Consultants Limited 6870 Goreway Drive Mississauga, Ontario L4V ]P] ABSTRACT. Chironomus spp. larvae collected from sediments in the harbour at Port Hope, Ontario, had a greater incidence of mouth part deformities in the more heavily polluted inner harbour area (83%,33 of 40 individuals) than in the outer harbour (14%, 1 of 7 individuals). Port Hope Harbour, the site of radium and uranium refining operations since 1933, is contaminated by 238U and (to a lesser extent) 232Th decay chain radionuclides and several trace metals. This difference suggests that deformities are related to the areal extent of contamination. An estimated dose rate of 1 mGy/day in chironomids suggests that radiation may be a significant factor in the induction of deformities; however, heavy metals and elevated water temperatures may also be involved. ADDITIONAL INDEX WORDS: Radioactive wastes, radium radioisotopes, uranium, trace metals, benthos.

INTRODUCTION

aberrations. Stations from the remainder of the lake yielded more than 1,700 specimens, all of which appeared normal. Warwick (1980a) recovered remains of deformed chironomid larvae, with deformities similar to those described by Brinkhurst et al. (1968), from sediment cores collected in the Bay of Quinte. The percentage of deformed specimens of Chironomus and Procladius clearly increased in the most recent sediments. According to the sediment core chronology, the incidence of deformities increased from 0.09010 in the pre-European sediments to 1.06% at 4.5 cm (1951) and 1.99% in the 1972 chironomid population. In a study of the benthic community in Parry Sound, Georgian Bay, Hare and Carter (1976) found that 77% of Chironomus (s.s.)? cucini larvae had deformities of the mouthparts. Refuse entering Parry Sound Harbour during the past 100

In recent years, the occurrence of hyperplasia and neoplasia in fishes from the Great Lakes and other waters has received widespread attention (see reviews by Baumann 1984 and Black 1984). There is strong evidence that such morphological abnormalities also develop in benthos in response to contamination. Most studies on abnormalities in freshwater macroinvertebrates have examined the occurrence of deformities in Chironomidae. Brinkhurst et al. (1968) and Hamilton and Saether (1971) reported that specimens of Chironomus spp. collected from the western end of Lake Erie near the Maumee River mouth were badly deformed. The most conspicuous feature of these larvae was an exceedingly thick exoskeleton. The head capsules were also thickened and heavily pigmented, and the mouth parts exhibited a variety of

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DEFORMITIES IN CHIRONOMUS years from lumbering, smelting, and explosives industries, as well as urban sewage, has left the sediments visibly contaminated with oil, cinders, and sawmill leavings. The harbour was the site of a massive oil spill in 1950. Only one deformed specimen was found among 73 larvae examined from outside the harbour. In and near Parry Sound Harbour, single deformed specimens of Procladius sp. and Micropsectra sp. praecox group were also collected. Several other investigators also have reported deformities in Great Lakes chironomids. Bocsor et al. (1974) reported increased frequencies of deformed Chironomus in Black River Bay, Lake Ontario, and implicated pollution by agricultural and industrial toxicants as a probable causal factor. Crowther and Luoma (1984) reported the occurrence of deformed larvae of C. salinarius in a habitat impaired by pulp and paper mill discharges in Thunder Bay, Lake Superior. In a survey of benthic macroinvertebrates of the central basin of Lake Erie, Krieger (1984) reported that one specimen of Chironomus near the mouth of the Grand River at Fairport Harbor and two specimens of Procladius near the mouths of the Black River at Lorain and the Cuyahoga River at Cleveland possessed deformed menta or ligulae, respectively. The occurrence of deformed chironomids in polluted waters outside of the Great Lakes basin has been reported by Hamilton and Saether (1971), Koehn and Frank (1980), Warwick (1980b), Tennessen and Gottfried (1983), Cushman (1984), and Wiederholm (1984). DESCRIPTION OF STUDY AREA The Port Hope Harbour study area and sediment chemistry is described in detail elsewhere (Hart et al. 1986). Wastes from radium and uranium refining operations have contaminated the harbour sediments with radionuc1ides of the 238U and (to a lesser extent) 232Th decay chains. Refining and metal fabricating operations have contributed to heavy metal pollution. Concentrations of Fe, Cu, Pb, and Ni in the inner harbour sediments (geometric means 32.1 mg'g- l, 122 p.g'g-l, 483 p.g.-l, and 58 p.g'g-l, respectively) exceed concentrations reported in basin-wide surveys of river mouth and harbour sediments around the Great Lakes (Fitchko and Hutchinson 1975, Thomas and Mudroch 1979) and exceed concentrations in Parry Sound Harbour (Konasewich et al. 1978) by at least threefold.

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In an earlier benthic survey of the harbour, Cook and Veal (1968) noted that most of the chironomids from a station in the inner harbour had deformed head capsules, although the incidence of deformities was not quantified. As part of an intensive benthic and sediment survey of Port Hope Harbour in November 1984 (Hart et al. 1986), we collected specimens of Chironomus spp. to quantify the incidence of deformities in differentially polluted areas of the harbour. Radiation dose rates for chironomids from the most contaminated inner area were also calculated to determine if ionizing radiation could be a factor contributing to developmental abnormalities. METHODS Chironomidae larvae were collected for inspection of the sc1erotized mouth parts and antennae from benthic samples taken at 20 stations. These specimens were permanently mounted on microscope slides according to Warwick and Casey (1982). The radiation dose rate to chironomids living in Port Hope Harbour sediments was estimated from radionuc1ide activities in sediments following the approach outlined by IAEA (1976) for a cylindrical body form (5 x 2 mm), assuming uniform concentrations of radionuc1ides in the tissues equal to those in the sediments (Hart et al. 1986). RESULTS AND DISCUSSION A total of 40 specimens of Chironomus spp. were collected from the heavily contaminated turning basin area of the inner harbour, of which 33 (83%) had deformed menta. Seven were found in samples from the less contaminated sediments of the outer harbour, of which only one (14070) was deformed. A single specimen collected from the mouth of the Ganaraska River was also deformed. Deformities included various types of asymmetry, such as gaps in the labial plate (Fig. 1), missing lateral teeth, and extra processes or fused processes on the median or first lateral teeth. None of the specimens examined displayed antennal deformities. Representatives of three Chironomus larval types (C. thummi, C. anthracinus, and C. plumosus) were represented in the collections. In general, turning basin contamination exceeded that in the outer harbour by one order of magnitude; river sediments were relatively uncontaminated by radionuc1ides, but were contaminated by some metals (Hart et al. 1986). For example, geometric mean activities of 230Th (in the 238U

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FIG. 1. Head capsules of deformed (A) and normal (B) specimens of Chironomus sp. thummi type from Port Hope Harbour. Note the pronounced asymmetry in the labial plate of (A).

DEFORMITIES IN CHIRONOMUS

decay chain) were 6.78 Bql g (0.063-76.6 Bql g) in sediments of the inner harbour, 0.42 Bq/g (0.07-1.12 Bq/g) in the outer harbour, and 0.36 Bq/g in the Ganaraska River. 230Th, like its daughters in the decay chain (226Ra, 2lOpb, and 2IOPO) is primarily radiotoxic, while U is primarily chemotoxic. Geometric mean U concentrations were 92.5 Jlg'g-l (3.5-1280 Jlg.g-l) in the inner harbour sediments, 1.77 Jlg'g-l (1.2-3.7 Jlg'g-l) in the outer harbour, and 4.2 Jlg/g in the Ganaraska River. A direct relationship between the degree of sediment contamination and the incidence of deformities in Chironomus spp. is thus suggested. The frequency of deformities observed in Chironomus spp. from the turning basin apparently is the highest reported for natural populations of chironomids. Total abundance of Chironomidae may be slightly reduced in association with this high deformity incidence when the geometric means in the inner harbour (511m2) and outer harbour (681m 2) are compared. Chironomus spp., however, were more abundant in the inner harbour than outside. Habitat factors such as wave action (greater in the outer harbour), and sediment particle size and organic content (greater in the inner harbour) probably influence abundance. Chironomid densities at Port Hope are at the lower end of the range for shallow waters in Lake Ontario (Nalepa and Thomas 1976). Blaylock (1965) reported cytogenetic effects on chironomid larvae in the sediments of White Oak Creek, Tennessee, which were contaminated with reactor fission product radionuclides. He also noted possible deformities of the pre-anal gills in chironomids from the nearby Clinch River (Nelson and Blaylock 1963). The radiation dose rate to chironomids in Port Hope Harbour sediments is estimated at approximately 1 mGy/day, similar to that in White Oak Creek (6.3 mGy/day), and thus may contribute to the observed chironomid deformities. Other authors have reported minor changes in reproductive patterns of aquatic snails (Cooley 1973) and desert rodents (French et al. 1974) at chronic dose rates of approximately 6 mGy/day, but these effects were not considered detrimental to the populations involved. Non-radioactive chemical contaminants in Port Hope turning basin sediments could be involved in deformity induction. Maximum Cu concentrations of 6,600 Jlg'g-l exceed the sediment concentrations shown by Cairns et al. (1984) to induce mortality in Chironomus tentans, however less toxic heavy

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metals such as Pb and Ni could also have teratogenic effects, as evidenced in vertebrates (Shepard 1983). High temperature cooling waters entering the turning basin could also be involved, although the temperature differential between the turning basin and outer harbour was only 2°C at the time of chironomid collections. Studies are presently underway to determine whether deformities can be induced in chironomids using recognized genotoxicants in the laboratory and to explore the utility of using deformities in natural populations as a biomonitoring tool to evaluate sediment quality. Preliminary results suggest a dose-related induction of mouth part deformities by chronic embryo-larval treatment with ethyl methanesulfonate at 75-250 mg/L. However, data on transmission of deformities to untreated generations are limited due to poor adult emergence and inviability of egg masses obtained from parents treated as larvae in this dose range. More work is required at lower dose levels to determine whether observed deformities may have a heritable genetic basis. ACKNOWLEDGEMENTS

We thank M. J. Goffin and R. J. Maloney for their support in the design and undertaking of this study. All chironomid larvae were mounted by C. A. Casey. This study was jointly funded by Environment Canada and the Atomic Energy Control Board of Canada in a contract awarded to Beak Consultants Limited. REFERENCES Baumann, P. C. 1984. Cancer in wild freshwater fish populations with emphasis on the Great Lakes. J. Great Lakes Res. 10:251-253. Black, J. J. 1984. Aquatic animal neoplasia as an indicator for carcinogenic hazards to man. In Hazard

Assessment of Chemicals: Current Developments, Vol. 3, ed. J. Saxena, pp. 181-232. New York: Academic Press. Blaylock, B. G. 1965. Chromosomal abberations in a natural population of Chironomus tentans exposed to chronic low-level radiation. Evolution 19:421-429. Bocsor, J. G., Cross, P. K., and Moore, R. B. 1974. The benthic macroinvertebrate fauna of southeastern nearshore Lake Ontario, Oswego Harbor and Black River Bay. State University College at Oswego, New York, Lake Ontario Environmental Laboratory, unpublished manuscript. Brinkhurst, R. 0., Hamilton, A. L., and Herrington, H. B. 1968. Components of the bottom fauna of the

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St. Lawrence Great Lakes. University of Toronto, Great Lakes Institute Publications No. PR33. Cairns, M. A., Nebeker, A. V., Gakstatter, J. H., and Griffis, W. L. 1984. Toxicity of copper spiked sediments to freshwater invertebrates. Environ. Toxicol. and Chem. 3:435-445. Cook, W., and Veal, D. 1968. A preliminary biological survey of Port Hope Harbour. Ontario Water Resources Commission report. Cooley, J. L. 1973. Effects of chronic environmental radiation on a natural population of the aquatic snail Physa heterostropha. Radiation Res. 54:130-140. Crowther, R. A., and Luoma, M. E. 1984. Pattern recognition techniques to determine benthic and community responses to industrial input. Verh. Internat. Verein. Limnol. 22:2226-2231. Cushman, R. M. 1984. Chironomid deformities as indicators of pollution from a synthetic, coal-derived oil. Freshwater Biology 14:179-182. Fitchko, J., and Hutchinson, T. C. 1975. A comparative study of heavy metal concentrations in river mouth sediments around the Great Lakes. J. Great Lakes Res. 1:46-78. French, N. R., Maza, B. G., Hill, H. 0., Aschwarden, A. P., and Kaaz, H. W. 1974. A population study of irradiated desert rodents. Ecological Monographs 44:45-72. Hamilton, A. L., and Saether, O. A. 1971. The occurrence of characteristic deformities in the chironomid larvae of several Canadian lakes. Can. Ent. 103: 363-368. Hare, L., and Carter, J. C. H. 1976. The distribution of Chironomus (s.s.)? cucini (salinarius group) larvae (Diptera: Chironomidae) in Parry Sound, Georgian Bay, with particular reference to structural deformities. Can. J. Zool. 54:2129-2134. Hart, D. R., McKee, P. M., Burt, A. J., and Goffin, M. J. 1986. A benthic community and sediment quality assessment of Port Hope Harbour, Lake Ontario. J. Great Lakes Res. 12:206-220.' IAEA. 1976. Effects of ionizing radiation on aquatic organisms and ecosystems. International Atomic Energy Agency Technical Report Ser. 172, Vienna. Koehn, T., and Frank, C. 1980. Effect of thermal pollution in the chironomid fauna in an urban channel. In Chironomidae Ecology, Systematics, Cytology and Physiology, ed. D. A. Murray, pp. 187-194. Oxford: Pergamon Press.

Konasewich, D., Traversy, W., and Zar, H. 1978. Great Lakes Water Quality Board, Appendix E, Status Report on Organic and Heavy Metal Contaminants in the Lakes Erie, Michigan, Huron and Superior Basins. International Joint Commission, Windsor. Krieger, K. A. 1984. Benthic macroinvertebrates as indicators of environmental degradation in the southern nearshore zone of the central basin of Lake Erie. J. Great Lakes Res. 10:197-209. Nalepa, T. F., Thomas, N. A. 1976. Distribution of macrobenthic species in Lake Ontario in relation to sources of pollution and sediment parameters. J. Great Lakes Res. 2:150-163. Nelson, D. J., and Blaylock, B. G. 1963. The preliminary investigation of salivary gland chromosomes of Chironomus tentans Fabr. from the Clinch River. In Radioecology: Proceedings of the First National Symposium on Radioecology, pp. 367-372. AIBS. Reinhold Publ. Corp. Shepard, T. H. 1983. Catalog of Teratogenic Agents, Fourth Ed. Baltimore: Johns Hopkins University Press. Tennessen, K. J., and Gottfried, P. K. 1983. Variation and structure of ligula of Tanypodinae larvae (Diptera: Chironomidae). Ent. News. 94:109-116. Thomas, R. L., and Mudroch, A. 1979. Small Craft Harbours - sediment survey. Lakes Ontario, Erie and Lake St. Clair 1978. Dredging summary and protocol. Report to Small Craft Harbours Ontario Region from the Great Lakes Biolimnology Laboratory. Warwick, W. F. 1980a. Palaeolimnology of the Bay of Quinte, Lake Ontario: 2800 years of cultural influence. Fisheries and Oceans Canada, Can. Bull. Fish. Aquat. Sci. 206:1-117. ____ . 1980b. Pasqua Lake, southeastern Saskatchewan: A preliminary assessment of trophic status and contamination based on the Chironomidae (Diptera). In Chironomidae Ecology, Systematics, Cytology and Physiology, ed. D. A. Murray, pp. 255-267. Oxford: Pergamon Press. ____ , and Casey, C. A. 1982. Sampling chironomid communities in lakes. Environment Canada, Freshwater Institute, Publication No. NWRIW&NR-82-02. Wiederholm, T. 1984. Incidence of deformed chironomid larvae (Diptera: Chironomidae) in Swedish lakes. Hydrobiologia 109:243-249.