Quantifying variation and chemical correlates of bladderwrack quality - herbivore population makes a difference

Functional Ecology

Volumn 25, Issue 4, 2011, Pages 900-909

  Jormalainen, Veijo ^a   Koivikko, Riitta ^a   Ossipov, Vladimir ^a   Lindqvist, Meri ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

Ecological differentiation; Macroalga; Mesoherbivore; Metabolome; Phlorotannins; Plant herbivore interaction; Proteinic amino acid

Indexed keywords

AMINO ACID; BROWN ALGA; FOOD CONSUMPTION; GROWTH RATE; HERBIVORY; HOST QUALITY; INTERTIDAL ENVIRONMENT; ISOPOD; LIFE HISTORY TRAIT; MACROALGA; MARINE ECOSYSTEM; METABOLITE; PHYTOCHEMISTRY; PLANT-HERBIVORE INTERACTION; SEAWEED; SELECTION; TANNIN; WATER CONTENT;

ALGAE; FUCUS; FUCUS VESICULOSUS; IDOTEA BALTICA; PHAEOPHYCEAE;

EID: 79959853448     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2011.01841.x     Document Type: Article

References (74)

1. Agrawal, A.A., Lau, J.A. & Hamback, P.A. (2006) Community heterogeneity and the evolution of interactions between plants and insect herbivores. Quarterly Review of Biology, 81, 349-376.
2. Amarillo-Suarez, A.R. & Fox, C.W. (2006) Population differences in host use by a seed-beetle: local adaptation, phenotypic plasticity and maternal effects. Oecologia, 150, 247-258.
3. Amsler, C.D. & Fairhead, V.A. (2006) Defensive and sensory chemical ecology of brown algae. Advances in Botanical Research, 43, 1-91.
4. Amsler, C.D., Iken, K., McClintock, J.B., Amsler, M.O., Peters, K.J., Hubbard, J.M., Furrow, F.B. & Baker, B.J. (2005) Comprehensive evaluation of the palatability and chemical defenses of subtidal macroalgae from the Antarctic Peninsula. Marine Ecology-Progress Series, 294, 141-159.
5. Appel, H.M. (1993) Phenolics in ecological interactions - the importance of oxidation. Journal of Chemical Ecology, 19, 1521-1552.
6. Awmack, C.S. & Leather, S.R. (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47, 817-844.
7. Barbehenn, R.V. (2001) Roles of peritrophic membranes in protecting herbivorous insects from ingested plant allelochemicals. Archives of Insect Biochemistry and Physiology, 47, 86-99.
8. Barbehenn, R., Cheek, S., Gasperut, A., Lister, E. & Maben, R. (2005) Phenolic compounds in red oak and sugar maple leaves have prooxidant activities in the midgut fluids of Malacosoma disstria and Orgyia leucostigma caterpillars. Journal of Chemical Ecology, 31, 969-988.
9. Cogni, R. & Futuyma, D.J. (2009) Local adaptation in a plant herbivore interaction depends on the spatial scale. Biological Journal of the Linnean Society, 97, 494-502.
10. Coley, P.D. (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs, 53, 209-233.
11. Coley, P.D., Bateman, M.L. & Kursar, T.A. (2006) The effects of plant quality on caterpillar growth and defense against natural enemies. Oikos, 115, 219-228.
12. Cornell, H.V. & Hawkins, B.A. (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. American Naturalist, 161, 507-522.
13. Crispo, E. (2008) Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. Journal of Evolutionary Biology, 21, 1460-1469.
14. Cronin, G. (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theories. Marine Chemical Ecology (eds J.B. McClintock & B.J. Baker), pp. 325-353. CRC Press, London.
15. Cruz-Rivera, E. & Hay, M.E. (2001) Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation. Marine Ecology Progress Series, 218, 249-266.
16. Cruz-Rivera, E. & Hay, M.E. (2003) Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecological Monographs, 73, 483-506.
17. Duggins, D.O. & Eckman, J.E. (1997) Is kelp detritus a good food for suspension feeders? Effects of kelp species, age and secondary metabolites. Marine Biology, 128, 489-495.
18. Egan, S.P. & Ott, J.R. (2007) Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology, 88, 2868-2879.
19. Egas, M., Sabelis, M.W. & Dieckmann, U. (2005) Evolution of specialization and ecological character displacement of herbivores along a gradient of plant quality. Evolution, 59, 507-520.
20. Gandon, S. & Michalakis, Y. (2002) Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology, 15, 451-462.
21. Gols, R., Wagenaar, R., Bukovinszky, T., van Dam, N.M., Dicke, M., Bullock, J.M. & Harvey, J.A. (2008) Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology, 89, 1616-1626.
22. Greischar, M.A. & Koskella, B. (2007) A synthesis of experimental work on parasite local adaptation. Ecology Letters, 10, 418-434.
23. Gruner, D.S., Smith, J.E., Seabloom, E.W., Sandin, S., Ngai, J.T., Hillebrand, H., Harpole, W.S., Elser, J.J., Cleland, E.E., Bracken, M.E.S., Borer, E.T. & Bolker, B.M. (2008) A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecology Letters, 11, 1-16.
24. Haavisto, F., Välikangas, T. & Jormalainen, V. (2010) Induced resistance in a brown alga: phlorotannins, genotypic variation and fitness costs for the crustacean herbivore. Oecologia, 162, 685-695.
25. Harvey, J.A., van Nouhuys, S. & Biere, A. (2005) Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids. Journal of Chemical Ecology, 31, 287-302.
26. Haukioja, E. (2003) Putting the insect into the birch-insect interaction. Oecologia, 136, 161-168.
27. Haukioja, E., Ossipov, V. & Lempa, K. (2002) Interactive effects of leaf maturation and phenolics on consumption and growth of a geometrid moth. Entomologia Experimentalis et Applicata, 104, 125-136.
28. Hay, M.E., Duffy, J.E., Pfister, C.A. & Fenical, W. (1987) Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology, 68, 1567-1580.
29. Jormalainen, V., Honkanen, T. & Heikkilä, N. (2001) Feeding preferences and performance of a marine isopod on seaweed hosts: cost of habitat specialization. Marine Ecology Progress Series, 220, 219-230.
30. Jormalainen, V., Honkanen, T. & Vesakoski, O. (2008a) Geographical divergence in host use ability of a marine herbivore in alga-grazer interaction. Evolutionary Ecology, 22, 545-559.
31. Jormalainen, V. & Ramsay, T. (2009) Resistance of the brown alga Fucus vesiculosus to herbivory. Oikos, 118, 713-722.
32. Jormalainen, V., Wikström, S.A. & Honkanen, T. (2008b) Fouling mediates grazing - Intertwining of resistances to multiple enemies in the brown alga Fucus vesiculosus. Oecologia, 155, 559-569.
33. Jormalainen, V., Honkanen, T., Mäkinen, A., Hemmi, A. & Vesakoski, O. (2001) Why does herbivore sex matter? Sexual differences in utilization of Fucus vesiculosus by the isopod Idotea baltica. Oikos, 93, 77-86.
34. Jormalainen, V., Honkanen, T., Vesakoski, O. & Koivikko, R. (2005) Polar extracts of the brown alga Fucus vesiculosus (L.) reduce assimilation efficiency but do not deter the herbivorous isopod Idotea baltica (Pallas). Journal of Experimental Marine Biology and Ecology, 317, 143-157.
35. Karban, R. & Agrawal, A.A. (2002) Herbivore offense. Annual Review of Ecology and Systematics, 33, 641-664.
36. Kawecki, T.J. & Ebert, D. (2004) Conceptual issues in local adaptation. Ecology Letters, 7, 1225-1241.
37. Koivikko, R., Loponen, J., Pihlaja, K. & Jormalainen, V. (2007) High-performance liquid chromatographic analysis of phlorotannins from the brown alga Fucus vesiculosus. Phytochemical Analysis, 18, 326-332.
38. Kubanek, J., Lester, S.E., Fenical, W. & Hay, M.E. (2004) Ambiguous role of phlorotannins as chemical defenses in the brown alga Fucus vesiculosus. Marine Ecology Progress Series, 277, 79-93.
39. Li, Q., Eigenbrode, S.D., Stringham, G.R. & Thiagarajah, M.R. (2000) Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. Journal of Chemical Ecology, 26, 2401-2419.
40. Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D. & Schabenberger, O. (2006) SAS for Mixed Models, 2nd edn. SAS Institute Inc, Cary, NC.
41. Monro, K. & Poore, A.G.B. (2004) Selection in modular organisms: is intraclonal variation in macroalgae evolutionarily important? American Naturalist, 163, 564-578.
42. Nykänen, H. & Koricheva, J. (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos, 104, 247-268.
43. Pappers, S.M., van der Velde, G. & Ouborg, N.J. (2002) Host preference and larval performance suggest host race formation in Galerucella nymphaeae. Oecologia, 130, 433-440.
44. Poore, A.G.B. & Hill, N.A. (2006) Sources of variation in herbivore preference: among-individual and past diet effects on amphipod host choice. Marine Biology, 149, 1403-1410.
45. Poore, A.G.B. & Steinberg, P.D. (1999) Preference-performance relationships and effects of host plant choice in an herbivorous marine amphipod. Ecological Monographs, 69, 443-464.
46. Quinn, G.P. & Keough, M.J. (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.
47. Raubenheimer, D. & Simpson, S.J. (1999) Integrating nutrition: a geometrical approach. Entomologia Experimentalis et Applicata, 91, 67-82.
48. Riipi, M., Kause, A., Haukioja, E., Ossipov, V., Ossipova, S. & Pihlaja, K. (2005) Variable responses of folivorous sawflies to leaf quality of mountain birch. Canadian Journal of Forest Research-Revue Canadienne de Recherche Forestiere, 35, 189-198.
49. Schadler, M., Brandl, R. & Kempel, A. (2010) Host plant genotype determines bottom-up effects in an aphid-parasitoid-predator system. Entomologia Experimentalis et Applicata, 135, 162-169.
50. Schwaegerle, K.E., McIntyre, H. & Swingley, C. (2000) Quantitative genetics and the persistence of environmental effects in clonally propagated organisms. Evolution, 54, 452-461.
51. Shurin, J.B., Gruner, D.S. & Hillebrand, H. (2006) All wet or dried up? Real differences between aquatic and terrestrial food webs. Proceedings of the Royal Society B: Biological Sciences, 273, 1-9.
52. Sorensen, J.S. & Dearing, M.D. (2006) Efflux transporters as a novel herbivore countermechanism to plant chemical defenses. Journal of Chemical Ecology, 32, 1181-1196.
53. Sotka, E.E. (2005) Local adaptation in host use among marine invertebrates. Ecology Letters, 8, 448-459.
54. Sotka, E.E. & Hay, M.E. (2002) Geographic variation among herbivore populations in tolerance for a chemically rich seaweed. Ecology, 83, 2721-2735.
55. Sotka, E.E., Forbey, J., Horn, M., Poore, A.G.B., Raubenheimer, D. & Whalen, K.E. (2009) The emerging role of pharmacology in understanding consumer-prey interactions in marine and freshwater systems. Integrative and Comparative Biology, 49, 291-313.
56. Spitzer, B. (2006) Local maladaptation in the soft scale insect Saissetia coffeae (Hemiptera: Coccidae). Evolution, 60, 1859-1867.
57. Stamp, N. (2003) Out of the quagmire of plant defense hypotheses. The Quarterly Review of Biology, 78, 23-55.
58. Steinberg, P.D. & Van Altena, I.A. (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecological Monographs, 62, 189-222.
59. Stern, J.L., Hagerman, A.E., Steinberg, P.D. & Mason, P.K. (1996) Phlorotannin-protein interactions. Journal of Chemical Ecology, 22, 1877-1899.
60. Strauss, S.Y. (1997) Lack of evidence for local adaptations to individual plant clones or site by a mobile specialist herbivore. Oecologia, 110, 77-85.
61. Targett, N.M. & Arnold, T.M. (2001) Effects of secondary metabolites on digestion in marine herbivores. Marine Chemical Ecology (eds J.B. McClintock & B.J. Baker), pp. 391-412. CRC Press, Boca Raton, FL.
62. Targett, N.M., Boettcher, A.A., Targett, T.E. & Vrolijk, N.H. (1995) Tropical marine herbivore assimilation of phenolic rich plants. Oecologia, 103, 170-179.
63. Tatarenkov, A., Jonsson, R.B., Kautsky, L. & Johannesson, K. (2007) Genetic structure in populations of Fucus vesiculosus (Phaeophyceae) over spatial scales from 10m to 800km. Journal of Phycology, 43, 675-685.
64. Taylor, R.B. & Brown, P.J. (2006) Herbivory in the gammarid amphipod Aora typica: relationships between consumption rates, performance and abundance across ten seaweed species. Marine Biology, 149, 455-463.
65. Taylor, R.B., Sotka, E. & Hay, M.E. (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia, 132, 68-76.
66. Thompson, J.N. (2005) The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago.
67. Throop, H.L. & Lerdau, M.T. (2004) Effects of nitrogen deposition on insect herbivory: implications for community and ecosystem processes. Ecosystems, 7, 109-133.
68. Toth, G.B., Langhamer, O. & Pavia, H. (2005) Inducible and constitutive defenses of valuable seaweed tissues: consequences for herbivore fitness. Ecology, 86, 612-618.
69. Toth, G.B. & Pavia, H. (2007) Induced herbivore resistance in seaweeds: a meta-analysis. Journal of Ecology, 95, 425-434.
70. Trowbridge, C.D. (2004) Emerging associations on marine rocky shores: specialist herbivores on introduced macroalgae. Journal of Animal Ecology, 73, 294-308.
71. Vesakoski, O., Rautanen, J., Jormalainen, V. & Ramsay, T. (2009) Divergence in host use ability of a marine herbivore from two habitat types. Journal of Evolutionary Biology, 22, 1545-1555.
72. Wakefield, R.L. & Murray, S.N. (1998) Factors influencing food choice by the seaweed-eating marine snail Norrisia norrisi (Trochidae). Marine Biology, 130, 631-642.
73. Wright, J.T., de Nys, R., Poore, A.G.B. & Steinberg, P.D. (2004) Chemical defense in a marine alga: heritability and the potential for selection by herbivores. Ecology, 85, 2946-2959.
74. Zovi, D., Stastny, M., Battisti, A. & Larsson, S. (2008) Ecological costs on local adaptation of an insect herbivore imposed by host plants and enemies. Ecology, 89, 1388-1398.