Xenobiotic Impacts on the Skeletal System of Teleosts

  • Daniel J. Karen
  • Philippe E. Ross
  • Stephen J. Klaine
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 172)


The nervous and endocrine systems form closely related structures throughout the vertebrate body. For example, cholinergic and adrenergic neurons can affect hypothalamic signaling of the pituitary and modulate the hormonal axes governed by hypothalamic signals. Interfering with neuronal signal propagation on the neuron or at the synapse can therefore have serious implications regarding the health and well-being of affected organisms by disrupting normal neuroendocrine control of many homeostatic processes. Anthropogenic compounds, specifically organophosphate agents such as chlorpyrifos, have this potential. Ultimately, neurological changes or neuroendocrine disruption may alter skeletal structural integrity. Other xenobiotics, like organochlorines, may disrupt normal metabolic processes. Altered metabolic pathways may affect the composition of the skeletal system. Therefore, exposure to organophosphate and organochlorine pesticides may elicit changes in mechanical properties and composition of bone. In teleost fish, these effects have been observed in the field and reproduced in the laboratory.


Brook Trout Skeletal System Plasma Calcium Fathead Minnow Fundulus Heteroclitus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bjornsson BT, Haux C (1985) Distribution of calcium, magnesium, and inorganic phosphate of estradiol-17ß treated rainbow trout. J Comp Physiol B 155:347–352.CrossRefGoogle Scholar
  2. Bjornsson BT, Haux C, Bern HA, Deftos LJ (1989) 17ß-estradiol increases plasma calcitonin levels in salmonid fish. Endocrinology 125(4): 1754–1760.PubMedCrossRefGoogle Scholar
  3. Buckler DR, Witt A, Mayer FL, Huckins JN (1981) Acute and chronic effects of kepone and mirex on the fathead minnow. Trans Am Fish Soc 111:270–280.CrossRefGoogle Scholar
  4. Chakrabarti P, Mukherjee D (1993) Studies on the hypocalcemic actions of salmon calcitonin and ultimobranchial gland extracts in the freshwater teleost Cyprinus carpio. Gen Comp Endocrinol 90:267–273.PubMedCrossRefGoogle Scholar
  5. Couch JA, Winstead JT, Hanson DJ, Goodman LR (1979) Vertebral dysplasia in young fish exposed to the herbicide trifluralin. J Fish Dis 2:35–42.CrossRefGoogle Scholar
  6. Dabrowski K, El-Fiky N, Köck G, Frigg M, Wieser W (1990) Requirement and utilization of ascorbic acid and ascorbic sulfate in juvenile rainbow trout. Aquaculture 91: 317–337.CrossRefGoogle Scholar
  7. Dacke CG (1979) Calcium Regulation in Sub-Mammalian Vertebrates. Academic Press, New York.Google Scholar
  8. Davis WP (1988) Reproductive and developmental responses in the self-fertilizing fish, Rivulus marmoratus, induced by the plasticizer, di-n-butylphthalate. Environ Biol Fishes 21(2):81–90.CrossRefGoogle Scholar
  9. Davis WP (1997) Evidence for developmental and skeletal responses as potential signals of endocrine disrupting compounds in fishes. In: Rolland RM, Gilbertson M, Peterson RE (eds) Chemically Induced Alterations in Functional Development and Reproduction of Fishes. SETAC Press, Pensacola, FL.Google Scholar
  10. Ecobichon DJ (1996) Toxic effects of pesticides. In: Klaassen CD (ed) Casarett and Doull’s Toxicology: The Basic Science of Poisons. McGraw-Hill, New York.Google Scholar
  11. Fargher RC, McKeown BA (1989) The effect of prolactin on calcium homeostasis in Coho salmon (Oncorhynchus kitsuch). Gen Comp Endocrinol 73:398–403.PubMedCrossRefGoogle Scholar
  12. Fenwick JC, Lam TJ (1988) Effects of calcitonin on plasma calcium and phosphate in the mudskipper, Periophthalamodon schlossen (Teleosti), in water and during exposure to air. Gen Comp Endocrinol 70:224–230.PubMedCrossRefGoogle Scholar
  13. Fenwick JC, Verbost P (1993) A C-terminal fragment of the hormone stanniocalcin is bioactive in eels. Gen Comp Endocrinol 91:337–343.PubMedCrossRefGoogle Scholar
  14. Flik G, Fenwick JC, Kolar Z, Mayer-Gostan N, Wendelaar Bonga SE (1985) Whole body calcium flux rates in the cichlid teleost fish Oreochromis mossambicus adapted to fresh water. Am J Physiol. 249:R432-R437.PubMedGoogle Scholar
  15. Flik G, Perry SF (1989) Cortisol stimulates whole body calcium uptake and the brancial calcium pump in freshwater trout. J Endocrinol 120:75–82.PubMedCrossRefGoogle Scholar
  16. Flik G, Verbost PM (1993) Calcium transport in fish gills and intestine. Calcium regulation and signalling. J Exp Biol 184:17–29.Google Scholar
  17. Flik G, Labedz T, Lafeber FPJG, Wendelaar Bonga SE, Pang PKT (1989) Studies on teleost corpuscles of Stannius. Physiological and biochemical aspects of synthesis and release of hypocalcin in trout, goldfish, and eel. Fish Physiol Biochem 7:343–349.CrossRefGoogle Scholar
  18. Fraser RA, Kaneko T, Pang PKT, Harvey S (1991) Hypo- and hypercalcemic peptides in fish pituitary glands. Am J Physiol 260:R622–R626.PubMedGoogle Scholar
  19. Giesy JP, Solomon KR, Coates JR, Dixon KR, Giddings JM, Kenaga EE (1999) Chlor-pyrifos: Ecological risk assessment in North American aquatic environments. Rev Environ Contain Toxicol. 160:1–130.CrossRefGoogle Scholar
  20. Glimcher MJ (1960) Specificity of the molecular structure of organic matrices in mineralization. In: Calcification in Biological Systems: A Symposium Presented at the Washington Meeting of the American Association for the Advancement of Science, Washington, DC, December 29 1958, pp 421–487.Google Scholar
  21. Guyton AC, Hall JE (1996) Textbook of Medical Physiology. Saunders, Philadelphia.Google Scholar
  22. Hanssen RGJM, Aarden EM, van der Venne WPHG, Pang PKT, Wendelaar Bonga SE (1991) Regulation of secretion of the teleost fish hormone stanniocalcin, effects of extracellular calcium. Gen Comp Endocrinol 84:155–163.PubMedCrossRefGoogle Scholar
  23. Hanssen RGJM, Mayer-Gostan N, Flik G, Wendelaar Bonga SE (1992) Influence of ambient calcium levels on stanniocalcin secretion in the european eel (Anguilla anguilla). J Exp Biol 162:197–208.Google Scholar
  24. Herrmann-Erlee MPM, Flik G (1989) Endocrine involvement in bone metabolism. In: Vertebrate endocrinology: Fundamentals and biomedical implications. Volume 3: Regulation of calcium and phosphate. PKT Pang and MP Schreibman, Eds. Academic Press, Inc. NY. Pgs 211–242.Google Scholar
  25. Herrmann-Erlee MPM, van der Meer JM, Löwik CWCM, Van Leeuwen JPTM, Boonekamp PM (1988) Different roles for calcium and cyclic AMP in the action of PTH; Studies in bone expiants and isolated bone cells. Bone 9:93–100.PubMedCrossRefGoogle Scholar
  26. Huff RA, Abou-Donia MB (1995) In vitro effect of chlorpyrifos oxon on muscarinic receptors and adenylate cyclase. Neurotoxicology 16(2):281–290.PubMedGoogle Scholar
  27. Huff RA, Corcoran JJ, Anderson JK, Abou-Donia MB (1994) Chlorpyrifos oxon binds directly to muscarinic receptors and inhibits cAMP accumulation in rat striatum. J Pharmacol Exp Ther 269(1):329–335.PubMedGoogle Scholar
  28. Karen DJ, Draughn R, Fulton M, Ross PE (1998) Bone strength and acetylcholinesterase inhibition as endpoints in chlorpyrifos toxicity to Fundulus heteroclitus. Pestic Biochem Physiol 60:167–175.CrossRefGoogle Scholar
  29. Karen DJ, Ross PE, Klaine SJ (2001) Further considerations of the skeletal system as a marker of episodic chlorpyrifos exposure. Aquat Toxicol 52:285–296.PubMedCrossRefGoogle Scholar
  30. Kozlovskaya VI, Mayer FL (1984) Brain acetylcholinesterase and backbone collagen in fish intoxified with organophosphate pesticides. J Great Lakes Res 10(3):261–266.CrossRefGoogle Scholar
  31. Kozlovskaya VI, Mayer FL, Petti JD (1985) Acetylcholinesterase activity in the brain and collagen content in the vertebra of goldfish exposed to trichlorfon. J Hydrobiol 20:54–59.Google Scholar
  32. Kozlovskaya VI, Mayer FL, Menzikova OV, Chuyko GM (1993) Cholinesterases of aquatic animals. Rev Environ Contam Toxicol 132:117–142.CrossRefGoogle Scholar
  33. Krishnamurthy VG, Bern HA (1971) Innervation of the corpuscles of Stannius. Gen Comp Endocrinol 16:162–165.PubMedCrossRefGoogle Scholar
  34. Kühn K (1987) The classical collagens: Types I, II, and III. In: Mayne R, Burgeson References (eds) Structure and Function of Collagen Types. Academic Press, New York. p. 1–42.Google Scholar
  35. Lopez E (1970) L’os cellulaire d’un poisson téléostéen, Anguilla anguilla L. I. Etude histocytologique et histophysique. Z Zellforsch Mikrosk Anat. 109:552–565.PubMedCrossRefGoogle Scholar
  36. Lopez E, Peignoux-Deville J, Lallier F, Martelly E, Milet C (1976) Effects of calcitonin and ultimobranchialectomy (UBX) on calcium and bone metabolism in the eel, Anguilla anguilla L. Calcif Tiss Res. 20:173–186.CrossRefGoogle Scholar
  37. Löwik CWGM, Leeuwen JPTM, van der Meer JM, van Zeeland JK, Scheven BAA, Herrmann-Erlee MPM (1985) A two-receptor model for the action of parathyroid hormone on osteoblasts: a role for intracellular free calcium and cyclic AMP. Cell Calcium. 6:311–326.PubMedCrossRefGoogle Scholar
  38. Lu M, Wagner GF, Renfro JL (1994) Stanniocalcin stimulates phosphate reabsorption by flounder renal proximal tubule in primary culture. Am J Physiol 267:R1356–R1362.PubMedGoogle Scholar
  39. Mauck WL, Mehrle PM, Mayer FL (1978) Effects of polychlorinated Arochlor® 1254 on growth, survival, and bone development in brook trout (Salvelinus fontinalis). J Fish Res Board Can 35:1084–1088.CrossRefGoogle Scholar
  40. Mayer, FL, Mehrle PM, Dwyer WP (1975) Toxaphene effects on reproduction, growth, and mortality of brook trout. EPA-600/3–75-013. USEPA, Duluth, MN.Google Scholar
  41. Mayer FL, Mehrle PM, Dwyer WP (1977) Toxaphene: chronic toxicity to fathead minnow and channel catfish. EPA-600/3–77-069. USEPA, Duluth, MN.Google Scholar
  42. Mayer, FL, Mehrle PM, Crutcher PL (1978) Interactions of toxaphene and vitamin C in channel catfish. Trans Am Fish Soc 107(2):326–333.CrossRefGoogle Scholar
  43. Mayer FL, Mayer KS, Ellersieck MR (1986) Relation of survival to other endpoints in chronic toxicity tests with fish. Environ Toxicol Chem 5:737–748.CrossRefGoogle Scholar
  44. Mehrle PM, Mayer FL (1975a) Toxaphene effects on growth and bone composition of fathead minnows, Pimaphales promelas. J Fish Res Board Can 32:593–598.CrossRefGoogle Scholar
  45. Mehrle PM, Mayer FL (1975b) Toxaphene effects on growth and development of brook trout (Salvelinus fontinalis). J Fish Res Board Can 32:609–613.CrossRefGoogle Scholar
  46. Mehrle PM, Mayer FL, Buckler DR (1981) Kepone and mirex: effects on bone development and swim bladder composition in fathead minnows. Trans Am Fish Soc 110: 638–643.CrossRefGoogle Scholar
  47. Mehrle PA, Haines TA, Hamilton S, Ludke JL, Mayer FL, Ribick MA (1982) Relationship between body contaminants and bone development in east-coast striped bass. Trans Am Fish Soc 111:123–130.CrossRefGoogle Scholar
  48. Milliken CE, Fargher RC, Butkus A, McDonald M, Copp DH (1990) Effects of synthetic peptide fragments of teleocalcin (hypocalcin) on calcium uptake in juvenile rainbow trout (Salmo gairdneri). Gen Comp Endocrinol 77:416–422.PubMedCrossRefGoogle Scholar
  49. Norris WP, Chavin W, Lombard LS (1963) Studies of calcification in a marine teleost. Ann NY Acad Sci 109:312–336.PubMedCrossRefGoogle Scholar
  50. Richardson RJ (1995) Assessment of the neurotoxic potential of chlorpyrifos relative to other organophosphorus compounds: A critical review of the literature. J Toxicol Environ Health 44:135–165.PubMedCrossRefGoogle Scholar
  51. Sasayama Y, Suzuki N, Oguro C, Takei Y, Takahashi A, Watanabe TX, Nakajima K, Sakakibara S (1992) Calcitonin of the stingray: comparison of the hypocalcemic activity with other calcitonins. Gen Comp Endocrinol 86:269–274.PubMedCrossRefGoogle Scholar
  52. Shepherd GM (1988) Neurobiology. Oxford University Press, New York.Google Scholar
  53. Somogyi JC, Kodicek E (1969) Nutritional aspects of the development of bone and connective tissue. Proceedings of the Seventh Symposium of the Group of European Nutritionists. S. Karger Publishers, Basel, Switzerland.Google Scholar
  54. Srivastav AK, Srivastav SK, Sasayama Y, Suzuki N (1996) Corpuscles of stannius-ex-tract-induced rapid but transient hypocalcemia and hyperphosphatemia in stingray, Dasyatis akajei. Gen Comp Endocrinol 104:37–40.PubMedCrossRefGoogle Scholar
  55. Unsicker K, Polonais T, Lindmar R, Löffelholz K, Wolf U (1977) Catecholamines and 5-hydroxytryptamine in corpuscles of Stannius of the salmonid, Salmo irideus L. A study correlating electron microscopial, histochemical, and chemical findings. Gen Comp Endocrinol 31:121–132.PubMedCrossRefGoogle Scholar
  56. Verbost PM, Flik G, Fenwick JC, Greco AM, Pang PKT, Wendelaar Bonga SE (1993) Branchial calcium uptake: possible mechanisms of control by stanniocalcin. Fish Physiol Biochem 11:205–215.CrossRefGoogle Scholar
  57. Weiss RE, Watabe N (1979) Studies on the biology of fish bone. III. Ultrastructure of osteogenesis and resorption in osteocytic (cellular) and anosteocytic (acellular) bones. Calcif Tissue Int 28:43–56.PubMedCrossRefGoogle Scholar
  58. Wendelaar Bonga SE, van der Meij JCA, Krabben WAWA, Flik G (1984) The effect of water acidification on prolactin cells and pars intermidia PAS-positive cells in the teleost fish Oreochromis (formerly Sarotherodon) mossambicus and Carassius aura-tus. Cell Tissue Res. 238:601–609.Google Scholar
  59. Wendelaar Bonga SE, Lammers PI (1982) Effects of calcitonin on ultrastructure and mineral content of bone and scales of the cichlid teleost Sarotherodon mossambicus. Gen Comp Endocrinol. 48:60–70.PubMedCrossRefGoogle Scholar
  60. Wendelaar Bonga SE, Van der Meij JC (1980) The effect of ambient calcium on prolactin cell activity and plasma electrolytes in Sarothodon mossambicus. Gen Comp Endocrinol 44:391–401.CrossRefGoogle Scholar
  61. Wendelaar Bonga SE, Greven JA, Veenhuis M (1977) Vascularization, innervation, and ultrastructure of the endocrine cell types of Stannius corpuscles in the teleost Gaster-osteus aculeatus. J Morphol 153:225–243.CrossRefGoogle Scholar
  62. Withers PC (1992) Comparative Animal Physiology. Saunders, New York.Google Scholar

Copyright information

© Springer-Verlag 2001

Authors and Affiliations

  • Daniel J. Karen
    • 1
  • Philippe E. Ross
    • 2
  • Stephen J. Klaine
    • 3
  1. 1.ARCADIS JSALong BeachUSA
  2. 2.Environmental Engineering and ScienceColorado School of MinesGoldenUSA
  3. 3.Department of Environmental ToxicologyClemson UniversityPendletonUSA

Personalised recommendations