Costs of plasticity: responses to desiccation decrease post-metamorphic immune function in a pond-breeding amphibian
dc.contributor.author | Gervasi, Stephanie S. | en_US |
dc.contributor.author | Foufopoulos, Johannes | en_US |
dc.date.accessioned | 2010-06-01T21:24:43Z | |
dc.date.available | 2010-06-01T21:24:43Z | |
dc.date.issued | 2008-02 | en_US |
dc.identifier.citation | Gervasi, Stephanie S.; Foufopoulos, Johannes (2008). "Costs of plasticity: responses to desiccation decrease post-metamorphic immune function in a pond-breeding amphibian." Functional Ecology 22(1): 100-108. <http://hdl.handle.net/2027.42/74472> | en_US |
dc.identifier.issn | 0269-8463 | en_US |
dc.identifier.issn | 1365-2435 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/74472 | |
dc.description.abstract | 1. Phenotypic plasticity may allow an organism to respond to temporally variable opportunities for growth and risks of mortality. However, life-history theory assumes that there are often trade-offs between the benefits afforded by plasticity in one trait and the consequences of that plasticity on other traits that affect fitness. In organisms with a complex life cycle, trade-offs may occur between larval and post-metamorphic traits. 2. Many amphibians metamorphose in temporary ponds, and may accelerate larval development to avoid mortality when a pond desiccates. A younger age at metamorphosis often results in reduced body size, but may also facilitate a trade-off with physiological traits that are linked to fitness in the adult stage. 3. We investigated a potential trade-off between desiccation-driven acceleration of development rate and immune system responsiveness in a species that breeds exclusively in temporary ponds. We exposed Rana sylvatica (wood frog) tadpoles to four possible desiccation regimes and then assayed the cell-mediated immune response to a standardized foreign antigen, phytohaemagglutinin (PHA), injected 3 weeks after metamorphosis. We also quantified total leucocyte numbers from haematological smears to obtain a secondary measure of individual immunological condition. 4. Animals exposed to desiccation had shorter development times, weaker cellular immune system responses to PHA and lower total leucocyte numbers than animals from control groups. Both measures of immune response showed a decrease with increasing severity of the desiccation treatment. 5. It is currently unclear whether the observed depression in immune response is transient or permanent. However, even temporary periods of immune system suppression shortly after metamorphosis may lead to greater susceptibility to opportunistic pathogens or parasites. | en_US |
dc.format.extent | 187010 bytes | |
dc.format.extent | 3109 bytes | |
dc.format.mimetype | application/pdf | |
dc.format.mimetype | text/plain | |
dc.publisher | Blackwell Publishing Ltd | en_US |
dc.rights | Journal compilation © 2007 British Ecological Society | en_US |
dc.subject.other | Ephemeral Environment | en_US |
dc.subject.other | Phenotypic Plasticity | en_US |
dc.subject.other | Immune System | en_US |
dc.subject.other | Rana Sylvatica | en_US |
dc.title | Costs of plasticity: responses to desiccation decrease post-metamorphic immune function in a pond-breeding amphibian | en_US |
dc.type | Article | en_US |
dc.subject.hlbsecondlevel | Ecology and Evolutionary Biology | en_US |
dc.subject.hlbtoplevel | Science | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/74472/1/j.1365-2435.2007.01340.x.pdf | |
dc.identifier.doi | 10.1111/j.1365-2435.2007.01340.x | en_US |
dc.identifier.source | Functional Ecology | en_US |
dc.identifier.citedreference | Abrams, P.A., Leimar, O., Nylin, S. & Wiklund, C. ( 1996 ) The effect of flexible growth rates on optimal sizes and development times in a seasonal environment. American Naturalist, 147, 381 – 395. | en_US |
dc.identifier.citedreference | Alford, R.A. & Harris, R.N. ( 1988 ) Effects of larval growth history on anuran metamorphosis. American Naturalist, 131, 91 – 106. | en_US |
dc.identifier.citedreference | Altwegg, R. & Reyer, H-U. ( 2003 ) Patterns of natural selection on size at metamorphosis in water frogs. Evolution, 57, 872 – 882. | en_US |
dc.identifier.citedreference | Beck, C.W. & Congdon, J.D. ( 2000 ) Effects of age and size at metamorphosis on performance and metabolic rates of southern toad, Bufo terrestris, metamorphs. Functional Ecology, 14, 32 – 38. | en_US |
dc.identifier.citedreference | Berven, K.A. & Gill, D.E. ( 1983 ) Interpreting geographic variation in life-history traits. Integrative and Comparative Biology, 23, 85 – 97. | en_US |
dc.identifier.citedreference | Berven, K.A. ( 1981 ) Mate choice in the wood frog, Rana sylvatica. Evolution, 35, 707 – 722. | en_US |
dc.identifier.citedreference | Blanckenhorn, W.U. ( 1998 ) Adaptive phenotypic plasticity in growth, development, and body size in the yellow dung fly. Evolution, 52, 1394 – 1407. | en_US |
dc.identifier.citedreference | Bradshaw, W.E. & Johnson, K. ( 1995 ) Initiation of metamorphosis in the pitcher-plant mosquito: effects of larval growth history. Ecology, 76, 2055 – 2065. | en_US |
dc.identifier.citedreference | Chodorowski, A. ( 1969 ) The desiccation of ephemeral pools and the rate of development of Aedes communis larvae. Polish Archive for Hydrobiology, 16, 79 – 91. | en_US |
dc.identifier.citedreference | Collins, J.P. ( 1979 ) Intrapopulation variation in the body size at metamorphosis and timing of metamorphosis in the bullfrog, Rana catesbeiana. Ecology, 60, 738 – 749. | en_US |
dc.identifier.citedreference | Crespi, E.J. & Denver, R.J. ( 2005 ) Ancient origins of human developmental plasticity. American Journal of Human Biology, 17, 44 – 54. | en_US |
dc.identifier.citedreference | Cronje, P.B. ( 2003 ) Foetal programming of immune competence. Australian Journal of Experimental Agriculture, 43, 1427 – 1430. | en_US |
dc.identifier.citedreference | Crump, M.L. ( 1989 ) Effect of habitat drying on developmental time and size at metamorphosis in Hyla pseudopuma. Copeia, 1989, 794 – 797. | en_US |
dc.identifier.citedreference | Danks, H.V. ( 2006 ) Key themes in the study of seasonal adaptations in insects II. Life cycle patterns. Applied Entomology and Zoology, 41, 1 – 13. | en_US |
dc.identifier.citedreference | Daszak, P., Cunningham, A.A. & Hyatt, A.D. ( 2003 ) Infectious disease and amphibian population declines. Diversity and Distributions, 9, 141 – 150. | en_US |
dc.identifier.citedreference | Denver, R.J. ( 1997a ) Proximate mechanisms of phenotypic plasticity in amphibian metamorphosis. American Zoologist, 37, 172 – 184. | en_US |
dc.identifier.citedreference | Denver, R.J. ( 1997b ) Environmental stress as a developmental cue: corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Hormones and Behavior, 31, 169 – 179. | en_US |
dc.identifier.citedreference | Denver, R.J., Mirhadi, N. & Phillips, M. ( 1998 ) Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondi tadpoles to habitat desiccation. Ecology, 79, 1859 – 1872. | en_US |
dc.identifier.citedreference | Dhabhar, F.F. ( 2002 ) A hassle a day may keep the doctor away: stress and the augmentation of immune function. Integrative and Comparative Biology, 42, 556 – 564. | en_US |
dc.identifier.citedreference | Gerlanc, N.M. & Kaufman, G.A. ( 2005 ) Habitat of origin and changes in water chemistry influence development of western chorus frogs. Journal of Herpetology, 39, 254 – 265. | en_US |
dc.identifier.citedreference | Gilbertson, M.K., Haffner, G.D., Drouillard, K.G., Albert, A. & Dixon, B. ( 2003 ) Immunosuppression in the northern leopard frog ( Rana pipiens ) induced by pesticide exposure. Environmental Toxicology and Chemistry, 22, 101 – 110. | en_US |
dc.identifier.citedreference | Glennemeier, K.A. & Denver R.J. ( 2002 ) Developmental changes in interrenal responses in anuran amphibians. Integrative and Comparative Biology, 42, 565 – 573. | en_US |
dc.identifier.citedreference | Goater, C.P., Semlitsch, R.D. & Bernasconi, M.V. ( 1993 ) Effects of body size and parasite infection on the locomotory performance of juvenile toads, Bufo bufo. OIKOS, 66, 129 – 136. | en_US |
dc.identifier.citedreference | Gosner, K.L. ( 1960 ) A simplified table for staging anuran embryos and larvae. Herpetologica, 16, 183 – 190. | en_US |
dc.identifier.citedreference | Gotthard, K. & Nylin, S. ( 1995 ) Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos, 74, 3 – 17. | en_US |
dc.identifier.citedreference | Gotthard, K. ( 1998 ) Life history plasticity in the satyrine butterfly Lasiommata petropolitana: investigating an adaptive reaction norm. Journal of Evolutionary Biology, 11, 21 – 39. | en_US |
dc.identifier.citedreference | Harding, J.H. ( 1997 ) Amphibians and Reptiles of the Great Lakes Region. University of Michigan Press, Ann Arbor. | en_US |
dc.identifier.citedreference | Hentschel, B.T. & Emlet, R.B. ( 2000 ) Metamorphosis of barnacle nauplii: effects of food variability and a comparison with amphibian models. Ecology, 81, 3495 – 3508. | en_US |
dc.identifier.citedreference | Houghton, J.T., Ding, Y., Griggs, D.J., Noguer, M., van der Linden, P.J., Dai, X., Maskell, K. & Johnson, C.A. (eds) ( 2001 ) Climate Change 2001: The Scientific Basis. Cambridge University Press, Cambridge. | en_US |
dc.identifier.citedreference | Howard, R.D. ( 1980 ) Mating behavior and mating success in wood frogs, Rana sylvatica. Animal Behaviour, 28, 705 – 716. | en_US |
dc.identifier.citedreference | John-Alder, H.B. & Morin, P.J. ( 1990 ) Effects of larval density on jumping ability and stamina in newly metamorphosed Bufo woodhousii fowleri. Copeia, 1990, 856 – 860. | en_US |
dc.identifier.citedreference | Juliano, S.A. & Stoffregen, T.L. ( 1994 ) Effects of habitat drying on size at and time to metamorphosis in the tree hole mosquito Aedes triseriatus. Oecologia, 97, 369 – 376. | en_US |
dc.identifier.citedreference | Kikuyama, S., Kawamura, K., Tatanka, S. & Yamomoto, K. ( 1993 ) Aspects of amphibian metamorphosis – hormonal control. International Review of Cytology, 145, 105 – 148. | en_US |
dc.identifier.citedreference | Laurila, A. & Kujasalo, J. ( 1999 ) Habitat duration, predation risk and phenotypic plasticity in common frog ( Rana temporaria ) tadpoles. Journal of Animal Ecology, 68, 1123 – 1132. | en_US |
dc.identifier.citedreference | Lochmiller, R.L. & Deerenberg, C. ( 2000 ) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 87 – 98. | en_US |
dc.identifier.citedreference | Loman, J. & Claesson, D. ( 2003 ) Plastic response to pond drying in tadpoles Rana temporaria: test of cost models. Evolutionary Ecology Research, 5, 179 – 194. | en_US |
dc.identifier.citedreference | Loman, J. ( 1999 ) Early metamorphosis in common frog Rana temporaria tadpoles at risk of drying: an experimental demonstration. Amphibia-Reptilia, 20, 421 – 430. | en_US |
dc.identifier.citedreference | Longcore, J.R., Longcore, J.E., Pessier, A.P. & Halteman, W.A. ( 2007 ) Chytridiomycosis widespread in anurans of northeastern United States. Journal of Wildlife Management, 71, 435 – 444. | en_US |
dc.identifier.citedreference | Lounibos, P.L. ( 2001 ) Boom or bust development of a predatory mosquito in temporary aquatic habitats of Florida, USA. Israel Journal of Zoology, 47, 433 – 444. | en_US |
dc.identifier.citedreference | Low, B. ( 1976 ) The evolution of amphibian life histories in the desert. Evolution of Desert Biota (ed D.W. Goodall ), pp. 149 – 195. University of Texas Press, Austin. | en_US |
dc.identifier.citedreference | Lytle, D.A. ( 2001 ) Disturbance regimes and life history evolution. American Naturalist, 157, 525 – 536. | en_US |
dc.identifier.citedreference | McCormick, C.M., Smythe, J.W., Sharma, S. & Meaney, M.J. ( 1995 ) Sex-specific effects of prenatal stress on hypothalamic–pituitary–adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Developmental Brain Research, 84, 55 – 61. | en_US |
dc.identifier.citedreference | Merila, J., Laurila, A. & Lindgren, B. ( 2004 ) Variation in the degree and costs of adaptive phenotypic plasticity among Rana temporaria populations. Journal of Evolutionary Biology, 17, 1132 – 1140. | en_US |
dc.identifier.citedreference | Morey, S. & Reznick, D. ( 2000 ) A comparative analysis of plasticity in larval development in three species of spadefoot toads. Ecology, 81, 1736 – 1749. | en_US |
dc.identifier.citedreference | Morey, S.R. & Reznick, D.N. ( 2004 ) The relationship between habitat permanence and larval development in California spadefoot toads: field and laboratory comparisons of developmental plasticity. Oikos, 104, 172 – 190. | en_US |
dc.identifier.citedreference | Newman, R.A. & Dunham, A.E. ( 1994 ) Size at metamorphosis and water loss in a desert anuran ( Scaphiopus couchii ). Copeia, 1994, 372 – 381. | en_US |
dc.identifier.citedreference | Newman, R.A. ( 1988 ) Adaptive plasticity in development of Scaphiopus couchii tadpoles in desert ponds. Evolution, 42, 774 – 783. | en_US |
dc.identifier.citedreference | Newman, R.A. ( 1992 ) Adaptive plasticity in amphibian metamorphosis. Bioscience, 42, 671 – 678. | en_US |
dc.identifier.citedreference | Newman, R.A. ( 1994 ) Effects of changing density and food level on metamorphosis of a desert amphibian, Scaphiopus couchii. Ecology, 75, 1085 – 1096. | en_US |
dc.identifier.citedreference | Norris, K. & Evans, M.R. ( 2000 ) Ecological immunity: life history trade-offs and immune defense in birds. Behavioral Ecology, 11, 19 – 26. | en_US |
dc.identifier.citedreference | Nylin, S., Wickman, P.O. & Wiklund, C. ( 1989 ) Seasonal plasticity in growth and development of the speckled wood butterfly, Pararge aegeria (Satyrinae). Biological Journal of the Linnaean Society, 38, 155 – 171. | en_US |
dc.identifier.citedreference | Oppliger, A., Giorgi, M.S., Conelli, A., Nembrini, M. & John-Alder, H.B. ( 2004 ) Effect of testosterone on immunocompetence, parasite load, and metabolism in the common wall lizard ( Podarcis muralis ). Canadian Journal of Zoology, 82, 1713 – 1719. | en_US |
dc.identifier.citedreference | Ouellet, M., Mikaelian, I., Pauli, B.D., Rodrigue, J. & Green, D.M. ( 2005 ) Historical evidence of widespread chytrid infection in North American amphibian populations. Conservation Biology, 19, 1431 – 1440. | en_US |
dc.identifier.citedreference | Pfennig, D.W., Mabry, A. & Orange, D. ( 1991 ) Environmental causes of correlations between age and size at metamorphosis in Scaphiopus multiplicatus. Ecology, 72, 2240 – 2248. | en_US |
dc.identifier.citedreference | Rachowicz, L.J. & Vredenburg, V.T. ( 2004 ) Transmission of Batrachochytrium dendrobatids within and between amphibian life stages. Diseases of Aquatic Organisms, 61, 75 – 83. | en_US |
dc.identifier.citedreference | Relyea, R. ( 2002 ) Costs of phenotypic plasticity. American Naturalist, 159, 272 – 282. | en_US |
dc.identifier.citedreference | Reznick, D.N. ( 1990 ) Plasticity in age and size at maturity in male guppies ( Poecilia reticulata ): an experimental evaluation of alternative models of development. Journal of Evolutionary Biology, 3, 185 – 203. | en_US |
dc.identifier.citedreference | Roff, D.A. ( 1992 ) The Evolution of Life Histories: Theory and Analysis. Chapman & Hall, New York. | en_US |
dc.identifier.citedreference | Rollins-Smith, L.A. ( 1998 ) Metamorphosis and the amphibian immune system. Immunological Reviews, 166, 221 – 230. | en_US |
dc.identifier.citedreference | Rollins-Smith, L.A. ( 2001 ) Neuroendocrine–immune system interactions in amphibians. Implications for understanding global amphibian declines. Immunologic Research, 23, 273 – 280. | en_US |
dc.identifier.citedreference | Rollins-Smith, L.A., Parsons, S.C., Cohen, N. ( 1988 ) Effects of thyroxine-driven precocious metamorphosis on maturation of adult-type allograft rejection responsiveness in early thyroidectomized frogs. Differentiation, 37, 180 – 185. | en_US |
dc.identifier.citedreference | Rouf, M.A. ( 1969 ) Hematology of the leopard frog, Rana pipiens. Copeia, 1969, 682 – 687. | en_US |
dc.identifier.citedreference | Rowe, L. & Ludwig, D. ( 1991 ) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology, 72, 413 – 427. | en_US |
dc.identifier.citedreference | Rudolf, V.H.W. & Rodel, M-O. ( 2007 ) Phenotypic plasticity and optimal timing of metamorphosis under uncertain time constraints. Evolutionary Ecology, 21, 121 – 142. | en_US |
dc.identifier.citedreference | Sapolsky, R.M., Romero, L.M. & Munck, A.U. ( 2000 ) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21, 55 – 89. | en_US |
dc.identifier.citedreference | Schalm, O.W. ( 1986 ) Schalm's Veterinary Hematology, 4th edn. Lea and Febiger, Philadelphia. | en_US |
dc.identifier.citedreference | Sheldon, B.C. & Verhulst, S. ( 1996 ) Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends in Ecology and Evolution, 8, 317 – 321. | en_US |
dc.identifier.citedreference | Sheridan, M.A. & Kao, Y. ( 1998 ) Regulation of metamorphosis-associated changes in the lipid metabolism of selected vertebrates. American Zoologist, 38, 350 – 368. | en_US |
dc.identifier.citedreference | Skelly, D.K. & Werner, E.E. ( 1990 ) Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology, 71, 2313 – 2322. | en_US |
dc.identifier.citedreference | Smith, D.C. ( 1987 ) Adult recruitment in chorus frogs – effects of size and date at metamorphosis. Ecology, 68, 344 – 350. | en_US |
dc.identifier.citedreference | Smith-Gill, S.J. & Berven, K.A. ( 1979 ) Predicting amphibian metamorphosis. American Naturalist, 113, 563 – 585. | en_US |
dc.identifier.citedreference | Smits, J.E., Bortolotti, G.R. & Tella, J.L. ( 1999 ) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Functional Ecology, 13, 567 – 572. | en_US |
dc.identifier.citedreference | Stearns, S.C. ( 1976 ) Life-history tactics: a review of the ideas. Quarterly Review of Biology, 51, 3 – 47. | en_US |
dc.identifier.citedreference | Stearns, S.C. ( 1989a ) The evolutionary significance of phenotypic plasticity. Bioscience, 39, 436 – 445. | en_US |
dc.identifier.citedreference | Stearns, S.C. ( 1989b ) Trade-offs in life-history evolution. Functional Ecology, 3, 259 – 268. | en_US |
dc.identifier.citedreference | Stearns, S.C. ( 1992 ) The Evolution of life Histories. Oxford University Press, New York. | en_US |
dc.identifier.citedreference | Stoks, R., DeBlock, M., Slos, S., VanDoorslaer, W. & Rolff, J. ( 2006 ) Time constraints mediate predator-induced plasticity in immune function, condition, and life history. Ecology, 87, 809 – 815. | en_US |
dc.identifier.citedreference | Svensson, E., Sinervo, B. & Comendant, T. ( 2001 ) Density-dependent competition and selection on immune function in genetic lizard morphs. Proceedings of the National Academy of Sciences of the United States of America, 98, 12561 – 12565. | en_US |
dc.identifier.citedreference | Travis, J. ( 1984 ) Anuran size at metamorphosis: experimental test of a model based on intraspecific competition. Ecology, 65, 1155 – 1160. | en_US |
dc.identifier.citedreference | Twombly, S. ( 1996 ) Timing of metamorphosis in a freshwater crustacean: comparison with anuran models. Ecology, 77, 1855 – 1866. | en_US |
dc.identifier.citedreference | Van Buskirk, J. ( 1988 ) Interactive effects of dragonfly predation in experimental pond communities. Ecology, 69, 857 – 867. | en_US |
dc.identifier.citedreference | Watkins, T.B. ( 2001 ) A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life history traits in the pacific tree frog, Hyla regilla. Evolution, 55, 1668 – 1677. | en_US |
dc.identifier.citedreference | Weinstock, M., Matlina, E., Maor, G.I., Rosen, H. & McEwen, B.S. ( 1992 ) Prenatal stress selectively alters the reactivity of the hypothalamic–pituitary adrenal system in the female rat. Brain Research, 595, 195 – 200. | en_US |
dc.identifier.citedreference | Werner, E.E. ( 1986 ) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. American Naturalist, 128, 319 – 341. | en_US |
dc.identifier.citedreference | West-Eberhard, M.J. ( 1989 ) Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics, 20, 249 – 278. | en_US |
dc.identifier.citedreference | Whitaker, B.R. & Wright, K.N. ( 2001 ) Amphibian Medicine and Captive Husbandry. Krieger Publishing Co., Malabar. | en_US |
dc.identifier.citedreference | Wilbur, H.M. & Collins J.P. ( 1973 ) Ecological aspects of amphibian metamorphosis. Science, 182, 1305 – 1314. | en_US |
dc.identifier.citedreference | Wilbur, H.M. ( 1980 ) Complex life cycles. Annual Review of Ecology and Systematics, 11, 67 – 93. | en_US |
dc.identifier.citedreference | Wilbur, H.M. ( 1987 ) Regulation of structure in complex systems: experimental temporary pond communities. Ecology, 68, 1437 – 1452. | en_US |
dc.identifier.citedreference | Wilbur, H.M., Tinkle, D.W. & Collins, J.P. ( 1974 ) Environmental certainty, trophic level, and resource availability in life history evolution. American Naturalist, 108, 805 – 817. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.