Epidermal 'alarm substance' cells of fishes maintained by non-alarm functions: Possible defence against pathogens, parasites and UVB radiation

Proceedings of the Royal Society B: Biological Sciences

Volumn 274, Issue 1625, 2007, Pages 2611-2619

  Chivers, Douglas P ^a   Wisenden, Brian D ^b   Hindman, Carrie J ^a   Michalak, Tracy A ^a   Kusch, Robin C ^a   Kaminskyj, Susan G W ^a   Jack, Kristin L ^a   Ferrari, Maud C O ^a   Pollock, Robyn J ^a   Halbgewachs, Colin F ^a   Pollock, Michael S ^a   Alemadi, Shireen ^b   James, Clayton T ^c   Savaloja, Rachel K ^b   Goater, Cameron P ^c   Corwin, Amber ^b   Mirza, Reehan S ^d   Kiesecker, Joseph M ^e   Brown, Grant E ^f   Adrian Jr , James C ^g   Krone, Patrick H ^a   Blaustein, Andrew R ^h   Mathis, Alicia ⁱ   more..

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b MINNESOTA STATE UNIVERSITY MOORHEAD   (United States)

^c UNIVERSITY OF LETHBRIDGE   (Canada)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e THE NATURE CONSERVANCY   (United States)

^f Civil and Environmental Engineering   (Canada)

^g UNION COLLEGE   (United States)

^h OREGON STATE UNIVERSITY   (United States)

ⁱ MISSOURI STATE UNIVERSITY   (United States)

Author keywords

Alarm substance; Club cells; Immune function; Ostariophysi; Percidae; Schreckstoff

Indexed keywords

CADMIUM;

ALARM SIGNAL; CYTOLOGY; DEFENSE MECHANISM; FISH; IMMUNE RESPONSE; IMMUNE SYSTEM; NATURAL SELECTION; PARASITE; PATHOGEN; PREDATION; PREDATOR-PREY INTERACTION; SKIN; ULTRAVIOLET B RADIATION;

ARTICLE; BODY REGIONS; CELL DENSITY; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; EPIDERMIS CELL; FISH; IMMUNE FUNCTION TEST; NATURAL SELECTION; NONHUMAN; PREDATION RISK; PRIORITY JOURNAL; RADIATION EXPOSURE; SAPROLEGNIA; SKIN PENETRATION; TREMATODE; ULTRAVIOLET B RADIATION;

OOMYCETES; OSTARIOPHYSI; PERCIDAE; PISCES; SAPROLEGNIA; SAPROLEGNIA FERAX; SAPROLEGNIA PARASITICA; TREMATODA; UVULIFER;

EID: 34848831833     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2007.0709     Document Type: Article

References (46)

1. Al-Hassen, J. M., Thompson, M., Criddle, K. R., Summers, B. & Criddle, R. S. 1985 Catfish epidermal secretions in response to threat or injury: a novel defense response. Mar. Biol. 88, 117-123. (doi:10.1007/BF00397158)
2. Beakes, G. W., Wood, S. E. & Burr, A. W. 1994 Features which characterize Saprolegnia isolates from salmon fish lesions - a review. In Salmon saprolegniasis (ed. G. J. Mueller), pp. 33-66. Portland, OR: U.S. Department of Energy, Bonneville Power Administration.
3. Blaustein, A. R., Kiesecker, J. M., Chivers, D. P. & Anthony, R. G. 1997 Ambient UV-B radiation causes deformities in amphibian embryos. Proc. Natl Acad. Sci. USA 94, 13 735-13 737. (doi:10.1073/pnas.94.25.13735)
4. Blazer, V. S., Fabacher, D. L., Little, E. E., Ewing, M. S. & Kocan, K. M. 1997 Effects of ultraviolet-B radiation on fish: histologic comparison of a UVB-sensitive and a UVB-tolerant species. J. Aquat. Anim. Health 9, 132-143. (doi:10.1577/1548-8667(1997)009〈0132:EOUBRO〉2.3. CO;2)
5. Brown, G. E., Adrian Jr, J. C., Smyth, E., Leet, H. & Brennan, S. 2000 Ostariophysan alarm pheromones: laboratory and field tests of the functional significance of nitrogen oxides. J. Chem. Ecol. 26, 139-154. (doi:10.1023/A:1005445629144)
6. Bruno, D. W. & Wood, B. P. 1994 Saprolegnia and other oomycetes. In Fish diseases and disorders, vol. 3 (eds P. T. K. Woo & D. W. Bruno). Viral, bacterial and fungal infections, pp. 599-659. Wallingford, UK: CABI Publishing.
7. Chivers, D. P. & Mirza, R. S. 2001 Predator diet cues and the assessment of predation risk by aquatic vertebrates: a review and prospectus. In Chemical signals in vertebrates, vol. 9 (eds A. Marchlewska-Koj, J. J. Lepri & D. Müller-Schwarze), pp. 277-284. New York, NY: Plenum Press.
8. Chivers, D. P. & Smith, R. J. F. 1994 The role of experience and chemical alarm signalling in predator recognition by fathead minnows Pimephales promelas. J. Fish Biol. 44, 273-285. (doi:10.1111/j.1095-8649.1994.tb01205.x)
9. Chivers, D. P. & Smith, R. J. F. 1998 Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5, 338-352.
10. Chivers, D. P., Brown, G. E. & Smith, R. J. F. 1996 Evolution of chemical alarm signals: attracting predators benefits alarm signal senders. Am Nat. 148, 649-659. (doi:10.1086/285945)
11. Chivers, D. P., Zhao, X., Brown, G. E., Marchant, T. A. & Ferrari, M. C. O. In press. Predator-induced changes in morphology of a prey fish: the effects of food level and temporal frequency of predation risk. Evol. Ecol. (doi:10.1007/S10682-007-9182-8)
12. Danchin, É., Giraldeau, L.-A., Valone, T. J. & Wagner, R. H. 2004 Public information: from nosy neighbors to cultural evolution. Science 305, 487-491. (doi:10.1126/science.1098254)
13. Dill, B. C. & Fuller, M. S. 1971 Amino acid immobilization of fungal motile cells. Arch. Mikrobiol. 78, 92-98. (doi:10.1007/BF00409091)
14. Ferrari, M. C. O. & Chivers, D. P. 2006 Learning threat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information? Anim. Behav. 71, 19-26. (doi:10.1016/j.anbehav.2005.02.016)
15. Ferrari, M. C. O., Trowell, J. J., Brown, G. E. & Chivers, D. P. 2005 The role of leaning in the development of threat-sensitive predator avoidance in fathead minnows. Anim. Behav. 70, 777-784. (doi:10.1016/j. anbehav.2005.01.009)
16. Ferrari, M. C. O., Gonzalo, A., Messier, F. & Chivers, D. P. 2007 Generalization of learned predator recognition: an experimental test and framework for future studies. Proc. R. Soc. B 274, 1853-1859. (doi:10.1098/rspb.2007.0297)
17. Iger, Y. & Abraham, M. 1990 The process of skin healing in experimentally wounded carp. J. Fish Biol. 36, 421-437. (doi:10.1111/j.1095-8649.1990.tb05622.x)
18. Jensen, A. & Bro-Rasmussen, F. 1992 Environmental cadmium in Europe. Rev. Environ. Contam. Toxicol. 125, 101-181.
19. Kasumyan, A. O. & Ponomarev, V. Y. 1987 Biochemical features of alarm pheromone in fish of the order Cypriniformes. J. Evol. Biochem. Physiol. 23, 20-24.
20. Kiesecker, J. M., Belden, L. K., Shea, K. & Rubbo, M. J. 2004 Amphibian decline and emerging diseases. Am. Sci. 92, 138-147. (doi:10.1511/2004.2.138)
21. Lebedeva, N. E., Malyukina, G. A. & Kasumyan, A. O. 1975 The natural repellent in the skin of cyprinids. J. Ichthyol. 15, 472-480.
22. Lemly, A. D. & Esch, G. W. 1984 Effects of the trematode Uvulifer ambloplites on juvenile bluegill sunfish, Lepomis macrochirus: ecological implications. J. Parasitol. 70, 475-492. (doi:10.2307/3281395)
23. Magurran, A. E., Irving, P. W. & Henderson, P. A. 1996 Is there a fish alarm pheromone? A wild study and critique. Proc. R. Soc. B 263, 1551-1556. (doi:10.1098/rspb.1996.0227)
24. Mathis, A. & Smith, R. J. F. 1993 Chemical labeling of northern pike (Esox lucius) by the alarm pheromone of fathead minnows (Pimephales promelas). J. Chem. Ecol. 19, 1967-1979. (doi:10.1007/BF00983800)
25. Mathis, A., Chivers, D. P. & Smith, R. J. F. 1995 Chemical alarm signals: predator-deterrents or predator attractants? Am. Nat. 146, 994-1005. (doi:10.1086/285780)
26. Michalak, T. 2006 The effects of pathogens, parasites and familiarity on alarm cell investment in fathead minnows, Pimephales promelas. MSc thesis, University of Saskatchewan.
27. Nelson, J. S. 1994 Fishes of the world, 4th edn. New York, NY: Wiley-Interscience.
28. Pfeiffer, W. 1982 Chemical signals in communication. In Chemoreception in fishes, vol. 8 (ed. T. J. Hara). Developments in aquaculture and fisheries science, pp. 307-326. New York, NY: Elsevier.
29. Pfeiffer, W., Riegelbauer, G., Meir, G. & Scheibler, B. 1985 Effect of hypoxanthine-3(N)-oxide and hypoxanthine-1(N)-oxide on central nervous excitation of the black tetra Gymnocorymbus ternetzi (Characidae, Ostariophysi, Pisces) indicated by dorsal light response. J. Chem. Ecol. 11, 507-524. (doi:10.1007/BF00989562)
30. Pietrock, M. & Goater, C. P. 2005 Infectivity of Ornithodiplostomum ptychocheilus and Posthodiplostomum minimum (Trematoda: Diplostomidae) cercariae following exposure to cadmium. J. Parasitol. 91, 854-856. (doi:10.1645/GE-473R.1)
31. Pollock, M. S., Chivers, D. P., Mirza, R. S. & Wisenden, B. D. 2003 Fathead minnows learn to recognize chemical alarm cues of introduced brook stickleback. Environ. Biol. Fish. 66, 313-319. (doi:10.1023/A:1023905824660)
32. Ralphs, J. R. & Benjamin, M. 1992 Chondroitin and keratan sulfate in the epidermal club cells of teleosts. J. Fish Biol. 40, 473-475. (doi:10.1111/j.1095-8649.1992.tb02594.x)
33. Rex, M., Salawitch, R. J., von der Gathen, P., Harris, N. R. P., Chipperfield, M. P. & Naujokat, B. 2004 Arctic ozone loss and climate change. Geophys. Res. Lett. 31, L04116. (doi:10.1029/2003GL018844)
34. Richards, R. H. & Pickering, A. D. 1978 Frequency and distribution patterns of Saprolegnia infection in wild and hatchery-reared brown trout Salmo trutta L. and char Salvelinus alpinus (L). J. Fish Dis. 1, 69-82. (doi:10.1111/j.1365-2761.1978.tb00006.x)
35. Sanchez-Dardon, J., Voccia, I., Hontela, A., Chilmonczyk, S., Dunier, M., Boermans, H., Blakley, B. & Fournier, M. 1999 Immunomodulation by heavy metals tested individually or in mixtures in rainbow trout (Oncorhynchus mykiss) exposed in vivo. Environ. Toxicol. Chem. 18, 1492-1497. (doi:10.1897/1551-5028(1999)018〈1492:IBHMTI〉2.3.CO;2)
36. Sandland, G. T. & Goater, C. P. 2000 Development and intensity-dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). J. Parasitol. 86, 1056-1060.
37. Smith, R. J. F. 1992 Alarm signals in fishes. Rev. Fish Biol. Fish. 2, 33-63. (doi:10.1007/BF00042916)
38. Von Frisch, K. 1941 Über einen schreckstoff der fischhaut und seine biologische bedeutung. Z. Vergl. Physiol. 29, 46-149. (doi:10.1007/BF00304445)
39. Williams, G. C. 1992 Natural selection: domains, levels, and challenges. Oxford, UK: Oxford University Press.
40. Wisenden, B. D. 2003 Chemically-mediated strategies to counter predation. In Sensory processing in the aquatic environment (eds S. P. Collin & N. J. Marshall), pp. 236-251. New York, NY: Springer.
41. Wisenden, B. D. & Chivers, D. P. 2006 The role of public chemical information in antipredator behaviour. In Fish communication (eds F. Ladich, S. P. Collins, P. Moller & B. G. Kapoor), pp. 259-278. Enfield, NH: Science Publishers.
42. Wisenden, B. D. & Smith, R. J. F. 1997 The effect of physical condition and shoal-mate familiarity on proliferation of alarm substance cells in the epidermis of fathead minnows. J. Fish Biol. 50, 799-808. (doi:10.1111/j.1095-8649.1997.tb01973.x)
43. Wisenden, B. D. & Smith, R. J. F. 1998 A re-evaluation of the effect of shoalmate familiarity on the proliferation of alarm substance cells in fathead minnows. J. Fish Biol. 53, 841-846. (doi:10.1111/j.1095- 8649.1998.tb01837.x)
44. Wisenden, B. D. & Stacey, N. E. 2005 Fish semiochemicals and the evolution of communication networks. In Animal communication networks (ed. P. K. McGregor), pp. 540-567. Cambridge, UK: Cambridge University Press.
45. Wisenden, B. D. & Thiel, T. A. 2002 Field verification of predator attraction to minnow alarm substance. J. Chem. Ecol. 28, 433-438. (doi:10.1023/A:1017950628284)
46. Zaccone, G., Ainis, L., Fasulo, S., Mauceri, A., Lauriano, E. R., Licata, A. & Cascher, P. L. 1999 Paraneurons in the skin epithelium of the fishes. In Water/air transition in biology (eds A. K. Mittal, F. B. Eddy & J. S. Datta Munshi), pp. 188-213. New Delhi, India: Oxford and IBH Publishing.