Abstract
Environmental and/or genetic among-site variation in plant quality may influence growth and fecundity of specialized herbivores inhabiting a particular site. Such variation is important as it generates spatial variation in selection for traits related to plant–herbivore interaction. Littoral macroalgae are known to respond plastically to environmental variation by modifying their chemistry or morphology. We studied geographic variation in phlorotannin, nitrogen, protein, and sugar (fucose, mannitol, and melibiose) concentrations of the brown alga Fucus vesiculosus at 12 sites separated by 0.5 to 40 km in the naturally fragmented Archipelago Sea in the northern Baltic Sea. By this regional variation in algal chemistry we attempted to explain among-population variation in size and fecundity of the crustacean herbivore Idotea baltica. We observed high spatial variation in all the measured chemical characteristics of F. vesiculosus, as well as in female size and the number of eggs produced by the herbivores. Spatial variation in nitrogen or protein contents of the alga did not explain the variation of herbivore traits. However, egg size positively covaried with spatial variation in the concentration of mannitol, the major storage carbohydrate of the alga. Such a positive relationship may arise if I. baltica can utilize the nutritive value of a mannitol-rich diet thereby being better able to provision the developing eggs with energy-rich metabolites. Unexpectedly, the concentration of phlorotannins, secondary metabolites having a putative role in defense against herbivory, positively covaried with the size of the herbivore. Among-population variation in host plant chemistry and covariation of that with herbivore growth and reproduction imply that herbivores respond to the local quality of their host plants, and that geographical structuring of populations has to be taken into account in studies of plant–herbivore interactions.
Similar content being viewed by others
References
Arnold TM, Targett NM (2003) To grow and defend: lack of tradeoffs for brown algal phlorotannins. Oikos 100:406–408
Arnold TM, Tanner CE, Haych WI (1995) Phenotypic variation in polyphenolic content of the tropical brown alga Lobophora variegata as a function of nitrogen availability. Mar Ecol Prog Ser 123:177–183
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Chapman ARO (1995) Functional ecology of fucoid algae: twenty-three years of progress. Phycologia 34:132
Chapman ARO, Graigie JS (1978) Seasonal growth in Laminaria longicruris: relations with reserve carbohydrate storage and production. Mar Biol 46:209–213
Cole RG, Haggitt T (2001) Dietary preferences of Evechinus chloroticus and the persistence of the fucalean macroalga Carpophyllum flexuosum on coralline-dominated areas in northeastern New Zealand. In: Barker MF (ed) Echinoderms 2000. Swets and Zeitlinger, Lisse, pp 425–430
Coyer JA, Peters AF, Stam WT, Olsen JL (2003) Post-ice age recolonization and differentiation of Fucus serratus L. (Phaeophyceae; Fucaceae) populations in northern Europe. Mol Ecol 12:1817–1829
Cronin G, Hay ME (1996a) Effects of light and nutrient availability on the growth, secondary chemistry, and resistance to herbivory of two brown seaweeds. Oikos 77:93–106
Cronin G, Hay ME (1996b) Induction of seaweed chemical defenses by amphipod grazing. Ecology 77:2287–2301
Davis EM (1988) Protein assays: a review of common techniques. Am Biotechnol Lab 6:28–37
Deal MS, Hay ME, Wilson D, Fenical W (2003) Galactolipids rather than phlorotannins as herbivore deterrents in the brown seaweed Fucus vesiculosus. Oecologia 136:107–114
Einum S, Fleming IA (2000) Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405:565–567
Gibson J, Harwood CS (2002) Metabolic diversity in aromatic compound utilization by anaerobic microbes. Annu Rev Microbiol 56:345–369
Gómez I, Weykam G, Wiencke C (1998) Photosynthetic metabolism and major organic compounds in the marine brown alga Desmarestia menziensii from King George Island (Antarctica). Aquat Bot 60:105–118
Haahtela I (1978) Morphology as evidence of maturity in isopod Crustacea, as exemplified by Mesidotea entomon (L.). Ann Zool Fenn 15:186–190
Hammerström K, Dethier MN, Duggins DO (1998) Rapid phlorotannin induction and relaxation in five Washington kelps. Mar Ecol Prog Ser 165:293–305
Hartnoll RG (2001) Growth in Crustacea: twenty years on. Hydrobiologia 449:111–122
Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064
Hemmi A, Jormalainen V (2004) Genetic and environmental variation in performance of a marine isopod: effects of eutrophication. Oecologia (in press)
Hemmi A, Honkanen T, Jormalainen V (2004) Inducible resistance to herbivory in Fucus vesiculosus—duration, spreading and variation with nutrient availability. Mar Ecol Prog Ser (in press)
Honkanen T, Jormalainen V, Hemmi A, Mäkinen A, Heikkilä N (2001) Feeding and growth of the isopod Idotea baltica on the brown alga Fucus vesiculosus: roles of inter-population and within-plant variation in plant quality. Ecoscience 9:332–338
Honkanen T, Jormalainen V, Hemmi A, Mäkinen A, Heikkilä N (2002) Feeding and growth of the isopod Idotea baltica on the brown alga Fucus vesiculosus: roles of inter-population and within-plant variation in plant quality. Ecoscience 9: 332–338
Ilvessalo H, Tuomi J (1989) Nutrient availability and accumulation of phenolic compounds in the brown alga Fucus vesiculosus. Mar Biol 101:115–119
Jensen A (1956) Preliminary investigations of the carbohydrates of Laminaria digitata and Fucus serratus. Rep Norway Inst Seaweed Res 10:11
Jormalainen V, Honkanen T (2001) Multiple cues for phenotypic plasticity in phlorotannin production of the bladder wrack Fucus vesiculosus. Phycologia 40:59–60
Jormalainen V, Merilaita S, Tuomi J (1995) Differential predation on sexes affects colour polymorphism of the isopod Idotea baltica (Pallas). Biol J Linn Soc 55:45–68
Jormalainen V, Honkanen T, Heikkilä N (2001) Feeding preferences and performance of a marine isopod on seaweed hosts: cost of habitat specialization. Mar Ecol Prog Ser 220:219–230
Kalvas A, Kautsky L (1993) Geographical variation in Fucus vesiculosus morphology in the Baltic and North Seas. Eur J Phycol 28:85–91
Kingsolver JG, Pfennig DW, Servedio MR (2002) Migration, local adaptation and the evolution of plasticity. Trends Ecol Evol 17540–17541
Kornfeldt RA (1982) Relation between nitrogen and phosphorus content of macroalgae and the waters of northern Öresund. Bot Mar 25:197–201
Lehvo A, Bäck S, Kiirikki M (2001) Growth of Fucus vesiculosus L. (Phaeophyta) in the northern Baltic proper: energy and nitrogen storage in seasonal environment. Bot Mar 44:345–350
Lucas PW, Turner IM, Dominy NJ, Yamashita N (2000) Mechanical defenses to herbivory. Ann Bot 86:913–920
Lüning K, Schmitz K, Willenbrink J (1973) CO2-fixation and translocation in benthic marine algae III. Rates and ecological significance of translocation in Laminaria hyperborea and L. saccharina. Mar Biol 23:275–281
Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161
Panov VE, McQueen DJ (1998) Effects of temperature on individual growth rate and body size of a freshwater amphipod. Can J Zool 76:1107–1116
Paul VJ, Cruz-Rivera E, Thacker RW (2001) Chemical mediation of macroalgal-herbivore interactions: ecological and evolutionary perspectives. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, Fla., pp 227–265
Pavia H, Åberg P (1996) Spatial variation in polyphenolic content of Ascophyllum nodosum (Fucales, Phaeophyta). Hydrobiologia 326/327:199–203
Pavia H, Toth GB (2000a) Influence of light and nitrogen on the phlorotannin content of the brown seaweeds Ascophyllum nodosum and Fucus vesiculosus. Hydrobiologia 440:299–305
Pavia H, Toth G (2000b) Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212–3225
Pavia H, Cervin G, Lindgren A, Åberg P (1997) Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar Ecol Prog Ser 157:139–146
Pavia H, Toth GB, Lindgren A, Åberg P (2003) Intraspecific variation in the phlorotannin content of the brown alga Ascophyllum nodosum. Phycologia 42:378–383
Peckol P, Krane JM, Yates JL (1996) Interactive effects of inducible defense and resource availability on phlorotannins in the north Atlantic brown alga Fucus vesiculosus. Mar Ecol Prog Ser 138:209–217
Poore AGB, Steinberg PD (2001) Host-plant adaptation in an herbivorous marine amphipod: genetic potential not realized in field populations. Evolution 55:68–80
Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. In: Round FE, Chapman DJ (eds) Progress in phycological research, vol 4. Biopress, Bristol, UK, pp 129–241
Rice EL, Kenchington TJ, Chapman ARO (1985) Intraspecific geographic-morphological variation patterns in Fucus distichus and F. evanescens. Mar Biol 88:207–215
Roff DA (1992) The evolution of life histories—theory and analysis. Chapmann & Hall, New York
Ruuskanen A (2000) Ecological responses of Fucus vesiculosus L. along environmental gradients in the northern Baltic Sea. PhD thesis, University of Helsinki, Finland
Salemaa H (1979) Ecology of Idotea spp. (Isopoda) in the northern Baltic. Ophelia 18:133–150
SAS Institute (1990) SAS/STAT user’s guide: statistics, vers 8.01. SAS Institute, Cary, N.C.
Schink B, Philipp B, Muller J (2000) Anaerobic degradation of phenolic compounds. Naturwissenschaften 87:12–23
Shuster SM, Guthrie EE (1999) Effects of temperature and food availability on adult body length in natural and laboratory populations of Paracerceis sculpta (Holmes), a Gulf of California isopod. J Exp Mar Biol Ecol 233:269–284
Sotka EE, Hay ME (2002) Geographic variation among herbivore populations in tolerance for a chemically rich seaweed. Ecology 83:2721–2735
Steinberg PD (1988) The effects of quantitative and qualitative variation in phenolic compounds on feeding in three species of marine invertebrate herbivores. J Exp Mar Biol Ecol 120:221–237
Steinberg PD (1989) Biogeographical variation in brown algal polyphenolics and other secondary metabolites: comparison between temperate Australasia and North America. Oecologia 78:374–383
Steinberg PD, Van Altena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222
Stern JL, Hagerman AE, Steinberg PD, Mason PK (1996) Phlorotannin-protein interactions. J Chem Ecol 22:1877–1899
Suomela J, Ossipov V, Haukioja E (1995) Variation among and within mountain birch trees in foliage phenols, carbohydrates, and amino acids, and in growth of Epirrita autumnata larvae. J Chem Ecol 21:1421–1446
Swanson AK, Druehl LD (2002) Induction, exudation and the UV protective role of kelp phlorotannins. Aquat Bot 73:241–253
Targett N, Boettcher, AA, Targett TE, Vrolijk NH (1995) Tropical marine herbivore assimilation on phenolic-rich plants. Oecologia 103:170–179
Targett NM, Arnold TM (1998) Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34:195–205
Targett NM, Arnold TM (2001) Effects of secondary metabolites on digestion in marine herbivores. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, Fla., pp 391–412
Targett NM, Coen LD, Boettcher AA, Tanner CE (1992) Biogeographic comparisons of marine algal phenolics: evidence against a latitudinal trend. Oecologia 89:464–470
Taylor RB, Lindquist N, Kubanek J, Hay ME (2003) Intraspecific variation in palatability and defensive chemistry of brown seaweeds: effects on herbivore fitness. Oecologia 136:412–423
Thompson JN (1999a) Specific hypotheses on the geographical mosaic theory of coevolution. Am Nat 153:S1–S14
Thompson JN (1999b) Coevolution and escalation: are ongoing coevolutionary meanderings important? Am Nat 153:S92–S93
Van Alstyne KL (1988) Herbivore grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69:655–663
Van Alstyne KL (1995) The comparison of three methods for quantifying brown algal polyphenolic compounds. J Chem Ecol 21:45–58
Van Alstyne KL, Paul VJ (1990) The biogeography of polyphenolic compounds in marine macroalgae: temperate brown algal defenses deter feeding by tropical herbivorous fishes. Oecologia 84:158–163
Van Alstyne KL, McCarthy JJ III, Hustead CL, Duggins DO (1999) Geographic variation in polyphenolic levels of northeastern Pacific kelps and rockweeds. Mar Biol 133:371–379
Van Alstyne KL, Duggins DO, Dethier MN (2001) Spatial patterns in macroalgal chemical defenses. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, Fla., pp 301–324
Waterman PG, Mole S (eds) (1994) Analysis of phenolic plant metabolites. Blackwell Scientific, Oxford, UK
Winter FC, Estes JA (1992) Experimental evidence for the effects of polyphenolic compounds from Dictyoneurum californicum Ruprecht (Phaeophyta: Laminariales) on feeding rate and growth in the red abalone Haliotus rufenscens Swainson. J Exp Mar Biol Ecol 155:263–277
Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757–1766
Zimmer M (2002) Nutrition in terrestrial isopods (Isopoda: Oniscidea): an evolutionary-ecological approach. Biol Rev 77:455–493
Zimmer M, Danko JP, Pennings SC, Danford AR, Ziegler A, Uglow RF, Carefoot TH (2001) Hepatopancreatic endosymbionts in coastal isopods (Crustacea: Isopoda), and their contribution to digestion. Mar Biol 138:955–963
Zimmer M, Danko JP, Pennings SC, Danford AR, Ziegler A, Uglow RF, Carefoot TH (2002) Cellulose digestion and phenol oxidation in coastal isopods (Crustacea: Isopoda). Mar Biol 140:1207–1213
Zvyagintseva TN, Shevchenko NM, Chizhov AO, Krupnova TN, Sundukova EV, Isakov VV (2003) Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions. J Exp Mar Biol Ecol 294:1–13
Acknowledgements
We thank the Archipelago Research Institute, University of Turku for providing the facilities and Janne Eränen for assisting in the field and laboratory. Riitta Koivikko conducted the analyses of phlorotannins and sugars, and Katariina Yli-Hätälä the analyses of proteins. This study was financed by the Academy of Finland (#44086, #53832 and BIREME program).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Kühl, Helsingør
Rights and permissions
About this article
Cite this article
Hemmi, A., Jormalainen, V. Geographic covariation of chemical quality of the host alga Fucus vesiculosus with fitness of the herbivorous isopod Idotea baltica . Marine Biology 145, 759–768 (2004). https://doi.org/10.1007/s00227-004-1360-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-004-1360-4