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Effects of chronic exposure to acidified water on chemoreception of feeding stimuli in fathead minnows (Pimephales promelas): Mechanisms and ecological implications
A. Dennis Lemly,
R. J. F. Smith,
Corresponding Author
A. Dennis Lemly
Department of Biology, University of Saskatchewan Saskatoon, Saskatchewan, S7N 0W0 Canada
U.S. Fish and Wildlife Service, National Fisheries Contaminant Research Center, Route 1, Columbia, MO 65201Search for more papers by this authorR. J. F. Smith
Department of Biology, University of Saskatchewan Saskatoon, Saskatchewan, S7N 0W0 Canada
Search for more papers by this authorA. Dennis Lemly,
R. J. F. Smith,
Corresponding Author
A. Dennis Lemly
Department of Biology, University of Saskatchewan Saskatoon, Saskatchewan, S7N 0W0 Canada
U.S. Fish and Wildlife Service, National Fisheries Contaminant Research Center, Route 1, Columbia, MO 65201Search for more papers by this authorR. J. F. Smith
Department of Biology, University of Saskatchewan Saskatoon, Saskatchewan, S7N 0W0 Canada
Search for more papers by this authorAbstract
A computer-automated behavioral assay was used to assess the effects of reduced ambient pH on the response of fathead minnows to chemical feeding stimuli. The testing system quantified eight behavioral parameters based on the activity level of individual fish before and after exposure to a single-pulse dose of a feeding stimulus—a tissue culture medium (1 ml; Eagle minimum essential medium with Earl's salts and L-glutamine) — injected into the water circulation. Twentyfive adult minnows were tested after exposure to one of five pH levels: 8.0 (control), 7.0, 6.5, 6.0 and 5.5. Complete elimination of the feeding response occurred at pH = 6 and lower; responses at higher pH levels were not statistically different from those in the controls. Differences in water hardness (<10 mg/L CaCO3 versus > 160 mg/L CaCO3) and duration of exposure (72 h versus 30 d) had no influence on the pattern or degree of the pH effects. Scanning electron microscopy revealed no pathological or gross morphological correlates of the behavioral changes. To test for possible recovery, minnows that did not respond at pH = 6 were placed in water of control pH (8.0) for 24 h and then tested again; a statistically significant response to the feeding stimulus was restored. These results indicate that acute and chronic sublethal levels of acidification caused a reversible impairment of chemoreception and that the impairment can occur at a relatively high pH. The toxic effect probably involves mechanical and chemical inhibition of receptor cells in the olfactory and gustatory epithelia rather than actual destruction of chemosensory tissue. In nature, reduction of pH to approximately 6.0 could impair feeding behavior and reduce food intake, fecundity and long-term survival of fathead minnow populations. Our results correspond well with environmental studies that show that fathead minnows are eliminated from natural waters when pH levels reach 5.8 to 6.0.
References
- 1
Smith, R. J. F.
1977.
Chemical communication as adaptation: Alarm substance of fish.
In
D. Muller-Schwarze and
M. M. Mozell, eds.,
Chemical Signals in Vertebrates.
Plenum Press, NY,
pp. 303–320.
10.1007/978-1-4684-2364-8_17 Google Scholar
- 2 Atema, J. 1980. Chemical senses, chemical signals, and feeding behavior in fishes. In J. E. Bardach, J. J. Magnuson, R. C. May, and J. M. Reinhart, eds., Fish Behavior and Its Use in the Capture and Culture of Fishes. ICLARM Conference Proceedings 5. International Center for Living Aquatic Resources Management, Manila, Philippines, pp. 57–101.
- 3 Liley, N. R. 1982. Chemical communication in fish. Can. J. Fish. Aquat. Sci. 39: 22–35.
- 4 Hasler, A. D., A. T. Scholz and R. M. Horral. 1978. Olfactory imprinting and homing in salmon. Am. Scientist 66: 347–355.
- 5 Brannon, E. L., R. P. Whitman and T. P. Quinn. 1984. Responses of returning adult coho salmon to home water and population specific odors. Trans. Am. Fish Soc. 113: 374–377.
- 6 Foster, N. R. 1985. Lake trout reproductive behavior: Influence of chemosensory cues from young-of-the-year by-products. Trans. Am. Fish. Soc. 114: 794–803.
- 7 Smith, R. J. F. 1982. The adaptive significance of the alarm substance-fright reaction system. In T. J. Hara, ed., Chemoreception in Fishes. Elsevier, Amsterdam, pp. 327–342.
- 8 Pfeiffer, W. 1977. The distribution of fright reaction and alarm substance in fishes. Copeia, pp. 653–665.
- 9 Blaxter, J. S. H. 1980. Vision and the feeding of fishes. In J. E. Bardach, J. J. Magnuson, R. C. May and J. M. Reinhart, eds., Fish Behavior and Its Use in the Capture and Culture of Fishes. ICLARM Conference Proceedings 5. International Center for Living Aquatic Resources Management, Manila, Philippines, pp. 32–56.
- 10 Caprio, J. 1982. High sensitivity and specificity of olfactory and gustatory receptors of catfish to amino acids. In T. J. Hara, ed., Chemoreception in Fishes. Elsevier, Amsterdam, pp. 109–134.
- 11 Kasumyan, A. O. and N. I. Pashchenko. 1982. The role of olfaction in the defensive reaction of grass carp, Ctenopharyngodon idella (Cyprinidae), to alarm pheromone. J. Ichthyol. 22: 122–126.
- 12 Rehnberg, B. G. and C. B. Schreck. 1986. The olfactory L-serine receptor in coho salmon: Biochemical specificity and behavioral response. J. Comp. Physiol. (in press).
- 13 Jones, K. A. and T. J. Hara. 1985. Behavioral response of fishes to chemical cues: Results from a new bioassay. J. Fish. Biol. 27: 495–504.
- 14 Bloom, H. R., A. Perlmutter and R. J. Seeley. 1978. Effect of a sublethal concentration of zinc on an aggregating pheromone system in the zebrafish, Brachydanio rerio (Hamilton-Bachanan). Environ. Pollut. 17: 127–131.
- 15 Olsen, K. H. and L. B. Hoglund. 1985. Reduction by a surfactant of olfactory mediated attraction between juveniles of Arctic charr, Salvelinus alpinus (L.). Aquat. Toxicol. 6: 57–69.
- 16 Hara, T. J., S. B. Brown and R. E. Evans. 1983. Pollutants and chemoreception in aquatic organisms. In J. O. Nriagu, ed., Aquatic Toxicology Advances in Environmental Science and Technology, Vol. 13. John Wiley & Sons, New York, NY, pp. 247–306.
- 17 Lemly, A. D. and R. J. F. Smith. 1985. Effects of acute exposure to acidified water on the behavioral response of fathead minnows, Pimephales promelas, to chemical feeding stimuli. Aquat. Toxicol. 6: 25–36.
- 18 Kamchen, R. and T. J. Hara. 1980. Behavioral reactions of whitefish (Coregonus clupeaformis) to food extract: An application to sublethal toxicity bioassay. Can. Tech. Rept. Fish. Aquat. Sci. 975: 182–191.
- 19 Rehnberg, B. G. and C. B. Schreck. 1986. Acute metal toxicology of olfaction in coho salmon: Behavior, receptors, and odor-metal complexation. Bull. Environ. Contam. Toxicol. 36: 579–586.
- 20 Jones, K. A., T. J. Hara and E. Scherer. 1985. Behavioral modification in Arctic charr (Salvelinus alpinus) chronically exposed to sublethal pH. Physiol. Zool. 58: 400–412.
- 21 Sutterlin, A. M. 1974. Pollutants and the chemical senses of aquatic animals—Perspective and review. Chem. Senses Flavor 1: 167–178.
- 22 Gardner, G. R. 1975. Chemically induced lesions in estuarine or marine teleosts. In W. E. Ribelin and G. Migaki, eds., The Pathology of Fishes. University of Wisconsin Press, Madison, WI, pp. 657–693.
- 23 Fingerman, S. W. and E. C. Short, Jr. 1983. Changes in neurotransmitter levels in channel catfish after exposure to benzo(a)pyrene, naphthalene, and Aroclor 1254. Bull. Environ. Contam. Toxicol. 30: 147–151.
- 24 Fingerman, S. W. and L. C. Russell. 1980. Effects of the polychlorinated biphenyl Aroclor 1242 on locomotor activity and on the neurotransmitters dopamine and norepinephrine in the brain of the gulf killifish, Fundulus grandis. Bull. Environ. Contam. Toxicol. 25: 682–687.
- 25 Collier, T. K., M. M. Krahn and D. C. Malins. 1980. The disposition of naphthalene and its metabolites in the brain of rainbow trout (Salmo gairdneri). Environ. Res. 23: 35–41.
- 26 Brown, S. B., R. E. Evans, B. E. Thompson and T. J. Hara. 1982. Chemoreception and aquatic pollutants. In T. J. Hara, ed., Chemoreception in Fishes. Elsevier, New York, NY, pp. 363–393.
- 27 Lemly, A. D. and R. J. F. Smith. 1986. A behavioral assay for assessing effects of pollutants on fish chemoreception. Ecotoxicol. Environ. Safety 11: 210–218.
- 28 Sokal, R. R. and F. J. Rohlf. 1981. Biometry. W.H. Freeman, San Francisco, CA.
- 29 Tommesen, G. 1978. The spatial distribution of odour induced potentials in the olfactory bulb of char and trout (Salmonidae). Acta Physiol. Scand. 102: 205–217.
- 30 Tommesen, G. 1983. Detection of a blocking effect of low pH in the trout olfactory organ. In K. B. Doving, ed., Chemoreception in Studies of Marine Pollution. University of Oslo, Norway, pp. 44–48.
- 31 Hara, T. J. 1976. Effects of pH on the olfactory responses to amino acids in rainbow trout, Salmogairdneri. Comp. Biochem. Physiol. 54A: 37–39.
- 32 Hara, T. J. and S. MacDonald. 1976. Olfactory responses to skin mucous substances in rainbow trout, Salmo gairdneri. Comp. Biochem. Physiol. 54A: 41–44.
- 33 Daye, P. G. and E. T. Garside. 1976. Histopathologic changes in surficial tissues of brook trout, Salvelinus fontinalis (Mitchill), exposed to acute and chronic levels of pH. Can. J. Zool. 54: 2140–2155.
- 34 Fromm, P. O. 1980. A review of some physiological and toxicological responses of freshwater fish to acid stress. Environ. Biol. Fish. 5: 79–93.
- 35 Zuchelkowski, E. M., R. C. Lantz and D. E. Hinton. 1981. Effects of acid stress on epidermal mucus cells of brown bullhead Ictalurus nebulosus (Leseur): A morphometric study. Anat. Record 200: 33–39.
- 36 Miller, T. G. and W. C. MacKay. 1982. Relationship of secreted mucus to copper and acid toxicity in rainbow trout. Bull. Environ. Contam. Toxicol. 28: 68–74.
- 37 Ultsch, G. R. and G. Gros. 1979. Mucus as a diffusion barrier to oxygen: Possible role in O2 uptake at low pH in carp (Cyprinus carpio) gills. Comp. Biochem. Physiol. 62A: 685–690.
- 38 Shephard, K. L. 1982. The influence of mucus on the diffusion of ions across the esophagus of fish. Physiol. Zool. 55: 23–34.
- 39
Shepherd, K. L.
1981.
The influence of mucus on the diffusion of water across fish epidermis.
Physiol. Zool.
54:
224–229.
10.1086/physzool.54.2.30155823 Google Scholar
- 40 Lock, R. A. C. and A. P. van Overbeeke. 1981. Effects of mercuric chloride and methyl-mercuric chloride on mucus secretion in rainbow trout. Comp. Biochem. Physiol. 69C: 67–73.
- 41 Varansi, U., P. A. Robisch and D. C. Malins. 1975. Structural alterations in fish epidermal mucus produced by water-borne lead and mercury. Nature 258: 431–432.
- 42 Novoselov, V. I., L. D. Krapivinskaya and E. E. Fesenko. 1980. Molecular mechanisms of odor sensing. V. Some biochemical characteristics of the alanineous receptor from the olfactory epithelium of the skate Dasyatis pastinaca. Chem. Senses 5: 195–203.
- 43 Starrett, W. C. 1950. Food relationships of the minnows of the Des Moines River, Iowa. Ecology 32: 13–27.
- 44 Isaak, D. 1961. The ecological life history of the fathead minnow, Pimephales promelas (Rafinesque). Ph.D. thesis, University of Minnesota, St. Paul, MN.
- 45 Held, J. H. and J. J. Paterka. 1974. Age, growth, and food habits of the fathead minnow, Pimephales promelas, in North Dakota saline lakes. Trans. Am. Fish Soc. 103: 743–756.
- 46 Wetzel, R. G. 1975. Limnology. W.B. Saunders, Philadelphia, PA.
- 47 Mount, D. I. 1973. Chronic effect of low pH on fathead minnow survival, growth, and reproduction. Water Res. 7: 987–993.
- 48 Harvey, H. H. 1982. Population responses of fish in acidified waters. In R. E. Johnson, ed., Acid Rain/Fisheries. American Fisheries Society, Bethesda, MD, pp. 227–242.
- 49 Zischke, J. A., J. W. Arthur, K. J. Nordlie, R. O. Hermanutz, D. A. Standen and T. P. Henry. 1983. Acidification effects on macroinvertebrates and fathead minnows (Pimephales promelas) in outdoor experimental channels. Water Res. 17: 47–63.
- 50 Somers, K. M. and H. H. Harvey. 1984. Alteration of fish communities in lakes stressed by acid deposition and heavy metals near Wawa, Ontario. Can. J. Fish. Aquat. Sci. 41: 20–29.
- 51 Schindler, D. W., K. H. Mills, D. F. Malley, D. L. Findlay, J. A. Shearer, I. J. Davies, M. A. Turner, G. A. Linsey and D. R. Cruikshank. 1985. Long-term ecosystem stress: The effects of years of experimental acidification on a small lake. Science 228: 1395–1401.
- 52 Bagenal, T. B. 1967. A short review of fish fecundity. In S. D. Gerking, ed., The Biological Basis of Freshwater Fish Production. Blackwell, Oxford, pp. 89–111.
- 53 Wootton, R. J. 1979. Energy costs of egg production and environmental determinants of fecundity in teleost fishes. Symposia of the Zoology Society of London 44: 133–159.
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