DOI QR코드

DOI QR Code

Seasonal variation in kelp phlorotannins in relation to grazer abundance and environmental variables in the Alaskan sublittoral zone

  • Dubois, Angela (School of Fisheries and Ocean Sciences, University of Alaska Fairbanks) ;
  • Iken, Katrin (School of Fisheries and Ocean Sciences, University of Alaska Fairbanks)
  • Received : 2011.12.09
  • Accepted : 2012.01.29
  • Published : 2012.03.15

Abstract

Phlorotannins are common metabolites produced in kelps that can have deterrent functions against grazers. The factors dictating seasonal patterns of phlorotannin content in northeastern Pacific kelps are not well understood. This study assessed density and grazing of the gastropod Lacuna vincta on the annual canopy-forming kelp Nereocystis luetkeana and the perennial understory species Agarum clathratum, Saccharina latissima and S. groenlandica in Kachemak Bay, Alaska. In addition, we assessed seasonal patterns of environmental variables as possible drivers of phlorotannin concentrations. Phlorotannins occurred in all species, with overall lowest levels in N. luetkeana, and with different seasonal patterns among the four species. Lacuna vincta was most dense on N. luetkeana thalli in the summer and had highest grazing rates on this low-phlorotannin species. However, correlations between L. vincta density and phlorotannin content of each kelp species were not significant. Except for N. luetkeana, there were no correlations between phlorotannin levels and environmental variables. We suggest that kelp life history traits may be more important for phlorotannin patterns in these kelp species than grazers or environmental drivers.

References

  1. Amsler, C. D. 2001. Induced defenses in macroalgae: the herbivore makes a difference. J. Phycol. 37:353-356. https://doi.org/10.1046/j.1529-8817.2001.037003353.x
  2. Amsler, C. D. 2008. Algal chemical ecology. Springer-Verlag, Berlin, Heidelberg, 331 pp.
  3. Amsler, C. D. & Fairhead, V. A. 2006. Defensive and sensory chemical ecology of brown algae. Adv. Bot. Res. 43:1-91.
  4. Astrom, M. & Lundberg, P. 1994. Plant defence and stochastic risk of herbivory. Evol. Ecol. 8:288-298. https://doi.org/10.1007/BF01238279
  5. Begin, C., Johnson, L. E. & Himmelman, J. H. 2004. Macroalgal canopies: distribution and diversity of associated invertebrates and effects on the recruitment and growth of mussels. Mar. Ecol. Prog. Ser. 271:121-132. https://doi.org/10.3354/meps271121
  6. Bryant, J. P., Chapin, F. S. & Klein, D. R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357-368. https://doi.org/10.2307/3544308
  7. Carney, L. T., Waaland, J. R., Klinger, T. & Ewing, K. 2005. Restoration of the bull kelp Nereocystis luetkeana in nearshore rocky habitats. Mar. Ecol. Prog. Ser. 302:49-61. https://doi.org/10.3354/meps302049
  8. Chavanich, S. & Harris, L. G. 2002. The influence of macroalgae on seasonal abundance and feeding preference of a subtidal snail, Lacuna vincta (Montagu) (Littorinidae) in the Gulf of Maine. J. Molluscan. Stud. 68:73-78. https://doi.org/10.1093/mollus/68.1.73
  9. Chenelot, H. 2003. Factors affecting estuarine populations of Nereocystis luetkeana in Kachemak Bay, Alaska. School of Fisheries and Ocean Sciences, University of Alaska Fairbanks Fairbanks, AK, 178 pp.
  10. Chenelot, H. & Konar, B. 2007. Lacuna vincta (Mollusca, Neotaenioglossa) herbivory on juvenile and adult Nereocystis luetkeana (Heterokontophyta, Laminariales). Hydrobiologia 583:107-118. https://doi.org/10.1007/s10750-006-0484-6
  11. Cronin, G. 2001. Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theories. In McClintock, J. B. & Baker, B. J. (Eds.) Marine Chemical Ecology. CRC Press, Boca Raton, FL, pp. 325-354.
  12. Cronin, G. & Hay, M. E. 1996. Effects of light and nutrient availability on the growth, secondary chemistry, and resistance to herbivory of two brown seaweeds. Oikos 77:93-106. https://doi.org/10.2307/3545589
  13. Cruces, E., Huovinen, P. & Gomez, I. 2012. Phlorotannin and antioxidant responses upon short-term exposure to UV radiation and elevated temperature in three South Pacific kelps. Photochem. Photobiol. 88:58-66. https://doi.org/10.1111/j.1751-1097.2011.01013.x
  14. Cruz-Rivera, E. & Hay, M. E. 2003. Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol. Monogr. 73:483-506. https://doi.org/10.1890/0012-9615(2003)073[0483:PNQIWC]2.0.CO
  15. Dayton, P. K. 1985. Ecology of kelp communities. Annu. Rev. Ecol. Syst. 16:215-245. https://doi.org/10.1146/annurev.es.16.110185.001243
  16. Deal, M. S., Hay, M. E., Wilson, D. & Fenical, W. 2003. Galactolipids rather than phlorotannins as herbivore deterrents in the brown seaweed Fucus vesiculosus. Oecologia 136:107-114. https://doi.org/10.1007/s00442-003-1242-3
  17. Dean, T. A., Schroeter, S. C. & Dixon, J. D. 1984. Effects of grazing by two species of sea urchins (Strongylocentrotus franciscanus and Lytechinus anamesus) on recruitment and survival of two species of kelp (Macrocystis pyrifera and Pterygophora californica). Mar. Biol. 78:301-313. https://doi.org/10.1007/BF00393016
  18. Dethier, M. N., Williams, S. L. & Freeman, A. 2005. Seaweeds under stress: manipulated stress and herbivory affect critical life-history functions. Ecol. Monogr. 75:403-418. https://doi.org/10.1890/03-4108
  19. Dubois, A. D. 2006. Temporal and spatial distribution of grazers and kelp phlorotannins in Kachemak Bay, Alaska. MS thesis, School of Fisheries and Ocean Sciences, University of Alaska Fairbanks, Fairbanks, AK, USA, 166 pp.
  20. Duggins, D., Eckman, J. E., Siddon, C. E. & Klinger, T. 2001. Interactive roles of mesograzers and current flow in survival of kelps. Mar. Ecol. Prog. Ser. 223:143-155. https://doi.org/10.3354/meps223143
  21. Fairhead, V. A., Amsler, C. D., McClintock, J. B. & Baker, B. J. 2005. Variation in phlorotannin content within two species of brown macroalgae (Desmarestia anceps and D. menziesii) from the Western Antarctic Peninsula. Polar Biol. 28:680-686. https://doi.org/10.1007/s00300-005-0735-4
  22. Fralick, R. A., Turgeon, K. W. & Mathieson, A. C. 1974. Destruction of kelp populations by Lacuna vincta (Montagu). Nautilus 88:112-114.
  23. Geiselman, J. A. & McConnell, O. J. 1981. Polyphenols in brown algae Fucus vesiculosus and Ascophyllum nodosum: chemical defenses against the marine herbivorous snail, Littorina littorea. J. Chem. Ecol. 7:1115-1133. https://doi.org/10.1007/BF00987632
  24. Granado, I. & Caballero, P. 2001. Feeding rates of Littorina striata and Osilinus atratus in relation to nutritional quality and chemical defenses of seaweeds. Mar. Biol. 138:1213-1224. https://doi.org/10.1007/s002270100544
  25. Hamilton, J. G., Zangerl, A. R., DeLucia, E. H. & Berenbaum, M. R. 2001. The carbon-nutrient balance hypothesis: its rise and fall. Ecol. Lett. 4:86-95. https://doi.org/10.1046/j.1461-0248.2001.00192.x
  26. Hammerstrom, K., Dethier, M. N. & Duggins, D. O. 1998. Rapid phlorotannin induction and relaxation in five Washington kelps. Mar. Ecol. Prog. Ser. 165:293-305. https://doi.org/10.3354/meps165293
  27. Hay, M. E. 1996. Marine chemical ecology: what's known and what's next? J. Exp. Mar. Biol. Ecol. 200:103-134. https://doi.org/10.1016/S0022-0981(96)02659-7
  28. Hay, M. E., Kappel, Q. E. & Fenical, W. 1994. Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 75:1714-1726. https://doi.org/10.2307/1939631
  29. 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. 273:109-120. https://doi.org/10.3354/meps273109
  30. Herms, D. A. & Mattson, W. J. 1992. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67:283-335. https://doi.org/10.1086/417659
  31. Iken, K. 1999. Feeding ecology of the Antarctic herbivorous gastropod Laevilacunaria antarctica Martens. J. Exp. Mar. Biol. Ecol. 236:133-148. https://doi.org/10.1016/S0022-0981(98)00199-3
  32. Iken, K., Amsler, C. D., Amsler, M. O., McClintock, J. B. & Baker, B. J. 2009. Field studies on deterrent properties of phlorotannins in Antarctic brown algae. Bot. Mar. 52:547-557. https://doi.org/10.1515/BOT.2009.071
  33. Iken, K., Amsler, C. D., Hubbard, J. M., McClintock, J. B. & Baker, B. J. 2007. Allocation patterns of phlorotannins in Antarctic brown algae. Phycologia 46:386-395. https://doi.org/10.2216/06-67.1
  34. Johnson, C. R. & Mann, K. H. 1986. The importance of plant defense abilities to the structure of subtidal seaweed communities: the kelp Laminaria longicruris de la Pylaie survives grazing by the snail Lacuna vincta (Montagu) at high population densities. J. Exp. Mar. Biol. Ecol. 97:231-267. https://doi.org/10.1016/0022-0981(86)90244-3
  35. Jormalainen, V., Honkanen, T., Koivikko, R. & Eranen, J. 2003. Induction of phlorotannin production in a brown alga: defense or resource dynamics? Oikos 103:640-650. https://doi.org/10.1034/j.1600-0706.2003.12635.x
  36. Konar, B., Iken, K. & Edwards, M. 2009. Depth-stratified community zonation patterns on Gulf of Alaska rocky shores. Mar. Ecol. 30:63-73. https://doi.org/10.1111/j.1439-0485.2008.00259.x
  37. Koricheva, J. 2002. The carbon-nutrient balance hypothesis is dead: long live the carbon-nutrient balance hypothesis? Oikos 98:537-539. https://doi.org/10.1034/j.1600-0706.2002.980319.x
  38. Krumhansl, K. A. & Scheibling, R. E. 2011. Spatial and temporal variation in grazing damage by the gastropod Lacuna vincta in Nova Scotian kelp beds. Aquat. Biol. 13:163-173. https://doi.org/10.3354/ab00366
  39. Kubanek, J., Lester, S. E., Fenical, W. & Hay, M. E. 2004. Ambiguous role of phlorotannins as chemical defenses in the brown alga Fucus vesiculosus. Mar. Ecol. Prog. Ser. 277:79-93. https://doi.org/10.3354/meps277079
  40. Littler, M. M. & Littler, D. S. 1980. The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am. Nat. 116:25-44. https://doi.org/10.1086/283610
  41. Luder, U. H. & Clayton, M. N. 2004. Induction of phlorotannins in the brown macroalga Ecklonia radiata (Laminariales, Phaeophyta) in response to simulated herbivory: the first microscopic study. Planta 218:928-937. https://doi.org/10.1007/s00425-003-1176-3
  42. Macaya, E. C. & Thiel, M. 2008. In situ tests on inducible defenses in Dictyota kunthii and Macrocystis integrifolia (Phaeophyceae) from the Chilean coast. J. Exp. Mar. Biol. Ecol. 354:28-38. https://doi.org/10.1016/j.jembe.2007.10.005
  43. Maney, E. J. Jr. & Ebersole, J. P. 1990. Continuous reproduction and episodic recruitment of Lacuna vincta (Montagu, 1803) in the Gulf of Maine. Veliger 33:215-221.
  44. Martel, A. & Chia, F. S. 1991. Oviposition, larval abundance, in situ larval growth and recruitment of the herbivorous gastropod Lacuna vincta in kelp canopies in Barkley Sound, Vancouver Island (British Columbia). Mar. Biol. 110:237-247. https://doi.org/10.1007/BF01313709
  45. Molis, M., Körner, J., Ko, Y. W. & Kim, J. H. 2008. Specificity of inducible seaweed anti-herbivory defences depends on identity of macroalgae and herbivores. Mar. Ecol. Prog. Ser. 354:97-105. https://doi.org/10.3354/meps07255
  46. Molis, M., Körner, J., Ko, Y. W., Kim, J. H. & Wahl, M. 2006. Inducible responses in the brown seaweed Ecklonia cava: the role of grazer identity and season. J. Ecol. 94:243-249. https://doi.org/10.1111/j.1365-2745.2005.01058.x
  47. O'Clair, R. M. & Lindstrom, S. C. 2000. North Pacific seaweeds. Plant Press, Auke Bay, AK, 162 pp.
  48. Paul, V. J., Cruz-Rivera, E. & Thacker, R. W. 2001. Chemical mediation of macroalgal-herbivore interactions: ecological and evolutionary perspectives. In McClintock, J. B. & Baker, B. J. (Eds.) Marine Chemical Ecology. CRC Press, Boca Raton, FL, pp. 227-265.
  49. 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. https://doi.org/10.3354/meps157139
  50. Pavia, H. & Toth, G. B. 2000a. Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212-3225. https://doi.org/10.1890/0012-9658(2000)081[3212:ICRTHI]2.0.CO;2
  51. Pavia, H. & Toth, G. B. 2000b. Influence of light and nitrogen on the phlorotannin content of the brown seaweeds Ascophyllum nodosum and Fucus vesiculosus. Hydrobiologia 440:299-305. https://doi.org/10.1023/A:1004152001370
  52. Pavia, H. & Toth, G. B. 2008. Macroalgal models in testing and extending defense theories. In Amsler, C. D. (Ed.) Algal Chemical Ecology. Springer-Verlag, Berlin, Heidelberg, pp. 147-172.
  53. Pavia, H., Toth, G. B. & Aberg, P. 2002. Optimal defense theory: elasticity analysis as a tool to predict intraplant variation in defenses. Ecology 83:891-897. https://doi.org/10.1890/0012-9658(2002)083[0891:ODTEAA]2.0.CO
  54. Pavia, H., Toth, G. B., Lindgren, A. & Aberg, P. 2003. Intraspecific variation in the phlorotannin content of the brown alga Ascophyllum nodosum. Phycologia 42:378-383. https://doi.org/10.2216/i0031-8884-42-4-378.1
  55. Peterson, C. H. & Renaud, P. E. 1989. Analysis of feeding preference experiments. Oecologia 80:82-86. https://doi.org/10.1007/BF00789935
  56. Ragan, M. A. & Glombitza, K. W. 1986. Phlorotannins, brown algal polyphenols. Prog. Phycol. Res. 4:130-241.
  57. Rhoades, D. F. 1979. Evolution of plant chemical defense against herbivores. In Rosenthal, G. A. & Janzen, D. H. (Eds.) Herbivores: Their Interactions With Secondary Plant Metabolites. Academic Press, New York, NY, pp. 3-54.
  58. Scheibling, R. E., Hennigar, A. W. & Balch, T. 1999. Destructive grazing, epiphytism, and disease: the dynamics of sea urchin-kelp interactions in Nova Scotia. Can. J. Fish. Aquat. Sci. 56:2300-2314. https://doi.org/10.1139/f99-163
  59. Schoenwaelder, M. E. A. & Clayton, M. N. 1999. The presence of phenolic compounds in isolated cell walls of brown algae. Phycologia 38:161-166. https://doi.org/10.2216/i0031-8884-38-3-161.1
  60. Stamp, N. 2003. Out of the quagmire of plant defense hypotheses. Q. Rev. Biol. 78:23-55. https://doi.org/10.1086/367580
  61. Steinberg, P. D. 1985. Feeding preferences of Tegula funebralis and chemical defenses of marine brown algae. Ecol. Monogr. 55:333-349. https://doi.org/10.2307/1942581
  62. Steinberg, P. D. 1994. Lack of short-term induction of phlorotannins in the Australasian brown algae Ecklonia radiata and Sargassum vestitum. Mar. Ecol. Prog. Ser. 112:129-133. https://doi.org/10.3354/meps112129
  63. Steinberg, P. D. & van Altena, I. 1992. Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol. Monogr. 62:189-222. https://doi.org/10.2307/2937093
  64. Steneck, R. S., Graham, M. H., Bourque, B. J., Corbett, D., Erlandson, J. M., Estes, J. A. & Tegner, M. J. 2002. Kelp bed ecosystems: biodiversity, stability, resilience and future. Environ. Conserv. 29:436-459.
  65. Steneck, R. S. & Watling, L. 1982. Feeding capabilities and limitation of herbivorous molluscs: a functional group approach. Mar. Biol. 68:299-319. https://doi.org/10.1007/BF00409596
  66. Stern, J. L., Hagerman, A. E., Steinberg, P. D., Winter, F. C. & Estes, J. A. 1996. A new assay for quantifying brown algal phlorotannins and comparisons to previous methods. J. Chem. Ecol. 22:1273-1293. https://doi.org/10.1007/BF02266965
  67. Svensson, C. J., Pavia, H. & Toth, G. B. 2007. Do plant density, nutrient availability, and herbivore grazing interact to affect phlorotannin plasticity in the brown seaweed Ascophyllum nodosum. Mar. Biol. 151:2177-2181. https://doi.org/10.1007/s00227-007-0649-5
  68. Targett, N. M. & Arnold, T. M. 1998. Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J. Phycol. 34:195-205. https://doi.org/10.1046/j.1529-8817.1998.340195.x
  69. Targett, N. M., Coen, L. D., Boettcher, A. A. & Tanner, C. E. 1992. Biogeographic comparisons of marine algal polyphenolics: evidence against a latitudinal trend. Oecologia 89:464-470. https://doi.org/10.1007/BF00317150
  70. Taylor, R. B., Sotka, E. & Hay, M. E. 2002. Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68-76. https://doi.org/10.1007/s00442-002-0944-2
  71. Toth, G. B. 2007. Screening for induced herbivore resistance in Swedish intertidal seaweeds. Mar. Biol. 151:1597-1604. https://doi.org/10.1007/s00227-007-0605-4
  72. Toth, G. B., Langhamer, O. & Pavia, H. 2005. Inducible and constitutive defenses of valuable seaweed tissues: consequences for herbivore fitness. Ecology 86:612-618. https://doi.org/10.1890/04-0484
  73. Toth, G. B. & Pavia, H. 2002. Lack of phlorotannin induction in the kelp Laminaria hyperborea in response to grazing by two gastropod herbivores. Mar. Biol. 140:403-409. https://doi.org/10.1007/s002270100707
  74. Toth, G. B. & Pavia, H. 2007. Induced herbivore resistance in seaweeds: a meta-analysis. J. Ecol. 95:425-434. https://doi.org/10.1111/j.1365-2745.2007.01224.x
  75. Tugwell, S. & Branch, G. M. 1989. Differential polyphenolic distribution among tissues in the kelps Ecklonia maxima, Laminaria pallida and Macrocystis angustifolia in relation to plant defense theory. J. Exp. Mar. Biol. Ecol. 129:219-230. https://doi.org/10.1016/0022-0981(89)90104-4
  76. Tuomi, J., Fagerstrom, T. & Niemela, P. 1991. Carbon allocation, phenotypic plasticity, and induced defenses. In Tallamy, D. W. & Raupp, M. J. (Eds.) Phytochemical Induction by Herbivores. John Wiley & Sons, New York, NY, pp. 85-104.
  77. Van Alstyne, K. L. 1988. Herbivore grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69:655-663. https://doi.org/10.2307/1941014
  78. Van Alstyne, K. L., McCarthy, J. J., Hustead, C. L. & Duggins, D. O. 1999. Geographic variation in polyphenolic levels of Northeastern Pacific kelps and rockweeds. Mar. Biol. 133:371-379. https://doi.org/10.1007/s002270050476
  79. Wikstrom, S. A. & Pavia, H. 2004. Chemical settlement inhibition versus post-settlement mortality as an explanation for differential fouling of two congeneric seaweeds. Oecologia 138:223-230. https://doi.org/10.1007/s00442-003-1427-9
  80. Yates, J. L. & Peckol, P. 1993. Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757-1766. https://doi.org/10.2307/1939934
  81. Zar, J. H. 1999. Biostatistical analysis. Prentice Hall, Upper Saddle River, NJ, 929 pp.

Cited by

  1. Foliose algal assemblages and deforested barren areas: phlorotannin content, sea urchin grazing and holdfast community structure in the Aleutian dragon kelp, Eualaria fistulosa vol.161, pp.10, 2014, https://doi.org/10.1007/s00227-014-2508-5
  2. Kelp in hot water: II. Effects of warming seawater temperature on kelp quality as a food source and settlement substrate vol.537, 2015, https://doi.org/10.3354/meps11421
  3. Seasonal and spatial variation in biochemical composition of Saccharina latissima during a potential harvesting season for Western Sweden vol.58, pp.6, 2015, https://doi.org/10.1515/bot-2015-0034
  4. The role of kelp species as biogenic habitat formers in coastal marine ecosystems vol.492, 2017, https://doi.org/10.1016/j.jembe.2017.01.017
  5. Seasonal Variations of Seaweed Community Structure at the Subtidal Zone of Bihwa on the East Coast of Korea vol.45, pp.3, 2012, https://doi.org/10.5657/KFAS.2012.0262
  6. Photosynthetic characteristics and UV stress tolerance of Antarctic seaweeds along the depth gradient vol.36, pp.9, 2013, https://doi.org/10.1007/s00300-013-1351-3
  7. Defensive role of macroalgal phlorotannins: benefits and trade-offs under natural herbivory vol.566, 2017, https://doi.org/10.3354/meps12004
  8. Isotopic evidence and consequences of the role of microbes in macroalgae detritus-based food webs vol.494, 2013, https://doi.org/10.3354/meps10544
  9. Effects of kelp phenolic compounds on the feeding-associated mobility of the herbivore snail Tegula tridentata vol.112, 2015, https://doi.org/10.1016/j.marenvres.2015.04.012
  10. Effect of upper beach macrofauna on nutrient cycling of sandy beaches: metabolic rates during wrack decay vol.165, pp.8, 2018, https://doi.org/10.1007/s00227-018-3392-1
  11. Biomolecular Composition and Revenue Explained by Interactions between Extrinsic Factors and Endogenous Rhythms of Saccharina latissima vol.17, pp.2, 2019, https://doi.org/10.3390/md17020107