Epidermal club cells do not protect fathead minnows against trematode cercariae: A test of the anti-parasite hypothesis

Biological Journal of the Linnean Society

Volumn 98, Issue 4, 2009, Pages 884-890

  James, Clayton T ^a,c   Wisenden, Brian D ^b   Goater, Cameron P ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

^b MINNESOTA STATE UNIVERSITY MOORHEAD   (United States)

^c Alberta Conservation Association   (Canada)

Author keywords

Alarm substance; Anti predation; Infectivity; Ornithodiplostomum; Ostariophysi; Pimephales

Indexed keywords

ALARM SIGNAL; ANTIPARASITE DEFENSE; EVOLUTIONARY BIOLOGY; FISH; INFECTIVITY; LARVA; SKIN;

CERCARIA (TREMATODE GENUS); ORNITHODIPLOSTOMUM; OSTARIOPHYSAN; OSTARIOPHYSI; PIMEPHALES; PIMEPHALES PROMELAS; PISCES; POECILIA; TREMATODA;

EID: 70450278684     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2009.01327.x     Document Type: Article

References (30)

1. Bahgat M, Ruppel A. 2002. Biochemical comparison of the serine protease (elastase) activities in cercarial secretions from Trichobilharzia ocellata and Schistosoma mansoni. Parasitology Research 88 : 495 500.
2. Ballabeni P, Ward PI. 1993. Local adaptation of the trematode Diplostomum phoxini to the European minnow, Phoxinus phoxinus, its second intermediate host. Functional Ecology 7 : 84 90.
3. Brown GE, Adrian JC, Smyth E, Leet H, Brennan S. 2000. Ostariophysan alarm pheromones: laboratory and field tests of the functional significance of nitrogen oxides. Journal of Chemical Ecology 26 : 139 154.
4. Buchmann K, Brescianni J. 1998. Microenvironment of Gyrodactylus derjvini on rainbow trout Oncorhynchus mykiss: association between mucous cell density in skin and site selection. Parasitology Research 84 : 17 24.
5. Carreau-Green ND, Mirza RA, Martinez ML, Pyle GG. 2008. The ontogeny of chemically mediated antipredator responses of fathead minnows Pimephales promelas. Journal of Fish Biology 73 : 2390 2401.
6. Chivers DP, Smith RJF. 1998. Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Écoscience 5 : 338 352.
7. Chivers DP, Wisenden BD, Hindman CJ, Michalak TA, Kusch RC, Kaminskyj SGW, Jack KL, Ferrari MCO, Pollock RJ, Halbgewachs CF, Pollock MS, Alemadi S, James CT, Savaloja RK, Goater CP, Corwin A, Mirza RS, Kiesecker JM, Brown GE, Krone PH, Blaustein AR, Mathis A. 2007. Epidermal 'alarm substance' cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation. Proceedings of the Royal Society of London Series B, Biological Sciences 274 : 2611 2619.
8. Haas W. 1994. Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success. Parasitology 109 : S15 S29.
9. Haas W, Wulff C, Grabe K, Meyer V, Haeberlein S. 2007. Navigation within host tissues: cues for orientation of Diplostomum spathaeceum (Trematoda) in fish towards veins, head, and eye. Parasitology 134 : 1013 1023.
10. Halbgewachs CF, Marchant TA, Kusch RC, Chivers DP. 2009. Epidermal club cells and the innate immune system of minnows. Biological Journal of the Linnean Society 98 : 891 897.
11. James SL. 1991. The effector function of nitrogen oxides in host defense against parasites. Experimental Parasitology 73 : 223 226.
12. James SL, Hibbs JB. 1990. The role of nitrogen oxides as effector molecules of parasitic killing. Parasitology Today 6 : 303 305.
13. James CT, Noyes KJ, Stumbo AD, Wisenden BD, Goater CP. 2008. Cost of exposure to trematode cercariae and learned recognition and avoidance of parasite risk by fathead minnows, Pimephales promelas. Journal of Fish Biology 73 : 2238 2248.
14. Kearn GC. 1999. The survival of monogenean (Platyhelminth) parasites on fish skin. Parasitology 119 : 57 88.
15. McKerrow JH, Slater J. 2002. Invasion of skin by Schistosome cercariae. Trends in Parasitology 18 : 193 195.
16. Magurran AE, Irving PW, Henderson PA. 1996. Is there a fish alarm pheromone? A wild study and critique. Proceedings of the Royal Society of London Series B, Biological Sciences 263 : 1551 1556.
17. Pfeiffer W. 1977. The distribution of fright reaction and alarm substance cells in fishes. Copeia 1977 : 653 665.
18. Pfeiffer W, Riegelbauer G, Meier 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. Journal of Chemical Ecology 11 : 507 523.
19. Poulin R. 2007. Evolutionary ecology of parasites, 2nd edn. Princeton, NJ : Princeton University Press.
20. Poulin R, Marcogliese DJ, McLaughlin JD. 1999. Skin-penetrating parasites and the release of alarm substances in juvenile rainbow trout. Journal of Fish Biology 55 : 47 53.
21. Sandland GJ, Goater CP. 2000. Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). Journal of Parasitology 86 : 1056 1060.
22. Sandland GJ, Goater CP, Danlychuk AJ. 2001. Population dynamics of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas) from four northern-Alberta lakes. Journal of Parasitology 87 : 744 748.
23. Shephard KL. 1994. Functions of fish mucus. Reviews in Fish Biology and Fisheries 4 : 401 429.
24. Smith RJF. 1982. Reaction of Percina nigrofasciata, Ammocrypti beani, and Etheostoma swaini (Percidae, Pisces) to conspecific and intergeneric skin extracts. Canadian Journal of Zoology 17 : 2253 2259.
25. Smith RJF. 1992. Alarm signals in fishes. Reviews in Fish Biology and Fisheries 2 : 33 63.
26. Whitear M. 1986. The skin of fishes including cyclostomes - epidermis. In : Bereiter-Hahn J, Matoltsy AG, Richards KS, eds. Biology of the integument. Heidelberg : Springer-Verlag, 8 38.
27. Williams GC. 1992. Natural selection: domains, levels, and challenges. New York, NY : Oxford University Press.
28. Wisenden BD, Smith RJF. 1997. The effect of physical condition and shoalmate familiarity on the proliferation of alarm substance cells in the epidermis of fathead minnows. Journal of Fish Biology 50 : 799 808.
29. Wisenden BD, Goater CP, James CT. 2009. Behavioral defenses against parasites and pathogens. In : Zaccone C, Perriere A, Mathis A, Kapoor G, eds. Fish defenses, Vol. 2. Enfield : Science Publishers, 151 168.
30. Zuk M, Stoehr AM. 2002. Immune defense and life history. American Naturalist 160 : 9 22.