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Factors Contributing to Variability in Club Cell Investment in a North American Cyprinid Fish Species

David George Lonzarich, Megan Meller, Rebecca Frank

Abstract


In many fish species, particularly those from the superorder Ostariophysi, individuals contain club cells in their epidermal tissue. These cells contain a chemical substance, which when released by injury during predation events, lead to stereotyped anti-predatory behaviors in nearby fish. Recent evidence concerning the evolutionary origins of this system have suggested that club cells are associated with innate immunity, and may serve to protect fish from parasite infestations and injury. In this study, we explored factors associated with variability in club cell investment from several populations of a North American cyprinid fish species (Creek Chub, Semotilus atromaculatus), with a primary goal to test the anti-parasite hypothesis in a natural setting. Using a path model approach, we evaluated the relative effects of fish length, mucous cell densities, epidermis thickness and parasite burden on club cell investment. Our model, which included all four independent variables, explained most of the variability in club cell densities for our fish (R2 = 0.80), and that fish length (acting either directly or indirectly on the other variables) explained most of this variability. Club cell densities were positively associated with parasite burden when examined in isolation of other factors, but in the path model, the effect of parasite burden on club cell investment was non-significant. Although we could not find support for the anti-parasite hypothesis in this study, our model indicates that, at least in this species, most of the variability in club cell investment is associated with characteristics of individual fish, and not the conditions of the environments in which they occur.


Keywords


Alarm Response; Fish; Club Cells

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References


Amos Development Corporation. 2007. Amos 16.0.1. http://amosdevelopment.com

Berra, T.M., Au, R.-J. 1978. Incidence of Black Spot Disease in Cedar Fork Creek, Ohio. Ohio Journal of Sciences 78:318-322

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. Journal of Aquatic Animal Health 9:132-143.

Brown, G.E., Chivers, D.P., Smith R.J.F. 1995. Fathead minnows avoid conspecific and heterospecific alarm pheromones in the faeces of northern pike. Journal of Fish Biology 47:387-393.

Buchmann, K., Bresciani, J. 1998. Microenvironment of Gyrodactylus derjavini on rainbow trout Oncorhynchus mykiss: association between mucous cell density in skin and site selection. Parasitology Research. 84:17-24.

Byrne, B.M. 2009. Structural Equation Modeling with AMOS: basic concepts, applications and programming. CRC Press.

Chivers, D.P., Brown, G.E., Smith, J.F. 1996. The Evolution of Chemical Alarm Signals: Attracting Predators Benefits Alarm Signal Senders. American Naturalist 148:649-659.

Chivers D.P., Wisenden, B.D., Hindman, C.J., Michalak, T.A., Kusch, R.C., Kaminskyj, S.G., Jack, K.L., Ferrari, M.C., Pollock, R.J., Halbgewachs, C.F., Pollock M.S., Alemadi, S., James, C.T., Savaloja, R.K., Goater, C.P., Corwin, A., Mirza, R.S., Kiesecker, J.M., Brown, G.E., Adrian, J.C. Jr, Krone, P.H., Blaustein, A.R., 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 B. 274: 2611-2619.

Diagnostic Instruments, Inc. 1998. SPOT Software (Version 2.1) [Software]. Sterling Heights, MI. SPOT Imaging Solutions.

Døving, K. B., Hamdani, E. H., Höglund, E., Kasumyan, A., Tuvikene, A. O. 2005. Review of the Chemical and Physiological Basis of Alarm Reactions in Cyprinids. Fish Chemosenses. editor/K. Reutter; B.G. Kapoor. Enfield, NH: Science Publishers, 2005. pp. 133-163

Evans, H.E., Mackiewicz, J.S. 1958. The Incidence and Location of Metacercarial Cysts (Trematoda: Strigeida) on 35 Species of Central New York Fishes. The Journal of Parasitology 44:231-235.

Fukunishi, Y., Masuda, R., Yamashita, Y. 2006. Ontogeny of tolerance to and avoidance of ultraviolet radiation in red sea bream Pagrus major and black sea bream Acanthopagrus schlegeli. Fisheries Science 72:356-363

Gall, B.G., Mathis, A. 2011.Ontogenetic Shift in Response to Amphibian Alarm Cues by Banded Sculpins (Cottus carolinae). Copeia 2011:5-8.

Grace, J. B., Bollen, K.A. 2008. Representing general theoretical concepts in structural equation models: the role of composite variables. Environmental and Ecological Statistics 15:191– 213.

Grace, J. B., Anderson, T.M., Olff, H., Scheiner, S.M. 2010. On the specification of structural equation models for ecological systems. Ecological Monographs 80:67–87.

Haas, W. 1994. Physiological analyses of host-finding behavior in trematode cercariae: Adaptations for transmission success. Parasitology 109: S15-S29.

Halbgewachs, C.F., Marchant, T.A., Kusch, R.C., Chivers, D.P. 2009. Epidermal Club Cells and the Innate Immune System. Biological Journal of the Linnean Society 98:891-897.

Hooper, D., Couglan, J.C., Mullen, M.R. 2008. Structural equation modelling: guidelines for determining model fit. Electronic Journal of Business Research Methods 6:53–60.

Hu, L., Bentler, P.M. 1999. Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Structural Equation Modeling 6:1–55.

Humason, G.L. 1979. Animal Tissue Techniques. San Francisco, CA. W. H. Freeman and Company.

Iger, Y., Abraham, M. 1990. The process of skin healing in experimentally wounded carp. Journal of Fish Biology 36:421-437.

Ingram, G. A. 1980. Substances involved in the natural resistance of fish to infection -- A review. Journal of Fish Biology 16:23-60.

James, C.T., Wisenden, B.D. Goater, C.P. 2009. Epidermal club cells do not protect fathead minnows against trematode cercariae: a test of the anti-parasite hypothesis. Biological Journal of the Linnean Society 98:884-890.

Júnior, A.B., Magalhães, E.J., Hoffman, A., Ide, L.M. 2010. Conspecific and heterospecific alarm substance induces behavioral responses in piau fish Leporinus piau. Acta Ethologica 13:119-126.

Kenny, D. A. 2000. Measuring Model Fit. URL: www.adv-energy.com/~dakenny/causalm.htm

MacCallum, R. C., Browne, M. W., Sugawara, H. M. 1996. Power analysis and determination of sample size for covariance structure modeling. Psychological Methods 12:130–149.

Manek, A. K., Ferrari, M.C.O., Pollock, R.J., Vicente, D, Weber, L.P., Chivers, D.P. 2013. Within and between population variation in epidermal club cell investment in a freshwater prey fish: A cautionary tale for evolutionary ecologists. PLoS ONE 8(3): e56689.

Mathis, A., Chivers, D.P., Smith, R.J.F. 1995. Chemical Alarm Signals: Predator Deterrents or Predator Attractants? American Naturalist 145:994-1005.

Michalak, T.A. 2006. The effects of pathogens, parasites, and familiarity on alarm cell investment in fathead minnows, Pimephales promelas. (Unpublished Master’s Thesis). University of Saskatchewan, Saskatchewan.

Päkk, P., Hussar, P., Paaver, T. 2011. Alterations of club cell activity in epidermis of common carp, Cyprinus carpio (Actinopterygii: Cypriniformes: Cyprinidae), due to infection by Ichthyophthirius multifiliis (Protista: Ciliphora). Acta Ichthyologica et Piscatoria 41(3):185-192.

Pfeiffer, W. 1960. Über die Schreckreaktion bei Fischen und die Herkunft des Schreckstoffes. Zeitschrift für vergleichende Physiologie. 43:578-614.

Pfeiffer, W. 1977. The distribution of fright reaction and alarm substance cells in fishes. Copeia 1977: 6653-665

Pfeiffer, W., Walz, U., Wolf, R., Mangold-Wernado, U. 1985. Effects of steroid hormones and other substances on alarm substance cells and mucous cells in the epidermis of the European minnow, Phoxinus phoxinus (L.), and other Ostariophysi (Pisces). Journal of Fish Biology 27:553-570.

Pollock, R.J., Pollock, M.S., Ferrrari, M.C.O., Kaminskyj, S.G.W., Chivers, D.P. 2012. Do fathead minnows, Pimephales promelas Rafinesque, alter their club cell investment in responses to variable risk of infection from Saprolegnia? Journal of Fish Diseases 35:249-254.

Quist, M.C., Bower, M.R., Hubert, W.A. 2007. Infection by a Black Spot-Causing Species of Uvuliferand Associated Opercular Alterations in Fishes from a High-Desert Stream in Wyoming. Diseases of Aquatic Organisms 78:129-136.

Rasband, W.S., ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/, 1997-2011.

Shephard, K.L. 1994. Functions for fish mucus. Reviews in Fish Biology and Fisheries 4:401-429.

Smith, R.J.F. 1976. Seasonal loss of alarm substance cells in North American cyprinoid fishes and its relation to abrasive spawning behaviour. Canadian Journal of Zoology 54 :1172-1182

Smith, R.J.F. 1982. The adaptive significance of the alarm substance—fright reaction system. In Hara, T.J., ed. Chemoreception in Fishes. Amsterdam: Elsevier, pp. 327–42.

Smith, R.J.F. 1992. Alarm Signals in Fishes. Reviews in Fish Biology and Fisheries 2:33-63.

Stabell, O.B., Vegusdal, A. 2010. Socializing makes thick-skinned individuals: on the density of epidermal alarm substance cells in cyprinid fish, the crucian carp (Carassius carassius). Journal of Comparative Physiology A. 196:639-647.

Vaughn, L.R. 1962. The Incidence and Location of Metacercarial Cysts (Neascus spp., “Black Spot”) on Species of Fishes in Clay County, Missouri. Bios 33:216-220.

von Frisch K. 1938. Zur Psychologie des Fische-Schwarmes. Naturwissenschaften 26:601-606.

Wisenden, B.D., Smith, R.J.F. 1997. The effect of physical condition and shoalmate familiarity on proliferation of alarm substance cells in the epidermis of fathead minnows. Journal of Fish Biology 50:799-808.

Wisenden, B. D., Thiel, T. A. 2002 Field verification of predator attraction to minnow alarm substance. Journal of Chemical Ecology 28, 433–438.




DOI: http://dx.doi.org/10.18686/fsa.v1i2.1132

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