Marine Biology

, Volume 156, Issue 4, pp 555–567 | Cite as

Seasonal stresses shift optimal intertidal algal habitats

  • Megan N. DethierEmail author
  • Susan L. Williams
Original Paper


We studied how the growth, reproduction, and survival of a common intertidal rockweed (Fucus distichus) varied across its tidal elevation at 14 sites around San Juan Island, Washington, USA in spring–summer and fall-winter seasons. We also measured a suite of environmental factors including temperature, light, emersion time, slope, fetch, and herbivory. To interpret the response of Fucus we included measurements of phlorotannins and carbon storage compounds (mannitol, laminarin). Growth and reproduction exhibited parallel patterns across tidal zones and sites. Tidal zone was a significant source of variation for many Fucus response variables, whereas variation between sites was high but not generally a significant factor explaining Fucus growth and physiology. Unexpectedly, the tidal zone in which Fucus achieved its highest growth and reproduction switched between seasons. High zone thalli grew and reproduced better than Mid zone thalli in fall but not in spring. This result can be explained by different combinations of factors influencing Fucus in each season. In spring, longer emersion times due to daytime low tides resulted in lower growth rates higher on the shore, likely due to carbon limitation. In fall during nighttime low tides, emersion and carbon limitation stresses were minimal. Overall, fall growth was lower than spring growth, but low fall light was not responsible. Instead, warmer average fall temperatures in the High zone apparently favored growth and reproduction relative to the Mid zone. In contrast, Mid zone thalli were subjected to more intense herbivory and hydrodynamic stress associated with wave exposure and steep substrata during the fall. At least for some seaweeds, living in the presumably more stressful high zone can actually confer higher integrated performance.


Tidal Height Wave Exposure Tidal Elevation High Zone Phlorotannin Content 



Many folks worked very hard to gather and help analyze these data, including during wretched night tides, especially A. Freeman, the Marvelous Megans (M. Ferguson and M. Johnson), C. Catton, and D. and P. Duggins. We thank the following: Director and staff of the Friday Harbor Laboratories (consistently wonderful support), numerous property owners on San Juan Island (access to their shorelines), Dr. Julia Kubanek (walking SLW through the phlorotannin purification), Dr. William Fenical (use of his laboratory), Drs. Nancy Targett and Tom Arnold (general phlorotannin advice), Claire Dominic and Albert Carranza (mannitol, laminarin extractions), Carissa Haug (nitrate data), Dr. Neil Willits (statistical consultations, multivariate data analyses), and Drs. Cynthia Hays and Matthew Bracken (comments on the manuscript). This research was funded by NSF grants #OCE 9901138, 98196078, and 0196078. Experiments comply with current laws of the country in which the experiments were performed. Contribution #2441 from the Bodega Marine Laboratory, University of California-Davis.


  1. Allender BM (1977) Ecological experimentation with the generations of Padina japonica Yamada (Dictyotales: Phaeophyta). J Exp Mar Biol Ecol 26:225–234CrossRefGoogle Scholar
  2. Ang PO Jr (1991) Age- and size-dependent growth and mortality in a population of Fucus distichus. Mar Ecol Prog Ser 78:173–187CrossRefGoogle Scholar
  3. Beck MW (1997) Inference and generality in ecology: current problems and an experimental solution. Oikos 78:265–273CrossRefGoogle Scholar
  4. Chapman ARO (1989) Abundance of Fucus spiralis and ephemeral seaweeds in a high eulittoral zone: effects of grazers, canopy and substratum type. Mar Biol 102:565–572CrossRefGoogle Scholar
  5. Chapman ARO (1995) Functional ecology of fucoid algae: twenty-three years of progress. Phycologia 34:1–32CrossRefGoogle Scholar
  6. Chapman ARO, Craigie JS (1978) Seasonal growth in Laminaria longicruris: relation with reserve carbohydrate storage and production. Mar Biol 46:209–213CrossRefGoogle Scholar
  7. Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theories. In: McClintock J, Baker B (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 325–354CrossRefGoogle Scholar
  8. Davison IR, Pearson GA (1996) Review: stress tolerance in intertidal seaweeds. J Phycol 32:197–211CrossRefGoogle Scholar
  9. Dayton PK (1971) Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–388CrossRefGoogle Scholar
  10. Dethier MN (1982) Pattern and process in tidepool algae: factors influencing seasonality and distribution. Bot Mar 25:55–66CrossRefGoogle Scholar
  11. Dethier MN, Williams SL, Freeman A (2005) Seaweeds under stress: manipulated stress and herbivory affect critical life history functions. Ecol Monogr 75:403–418CrossRefGoogle Scholar
  12. Duggins DO, Simenstad CA, Estes JA (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245:170–173CrossRefGoogle Scholar
  13. Edwards P (1977) An investigation of the vertical distribution of selected benthic marine algae with a tide-simulating apparatus. J Phycol 13:62–68Google Scholar
  14. Edyvean RGJ, Ford H (1984) Population biology of the crustose red alga Lithophyllum incrustans Phil. 3. The effects of local environmental variables. Biol J Linn Soc 23:365–374CrossRefGoogle Scholar
  15. Fortes MD, Lüning K (1980) Growth rates of North Sea macroalgae in relation to temperature, irradiance and photoperiod. Helgol Meeres 34:15–29CrossRefGoogle Scholar
  16. Foster MS (1990) Organization of macroalgal assemblages in the northeast Pacific: the assumption of homogeneity and the illusion of generality. Hydrobiologia 192:21–23CrossRefGoogle Scholar
  17. Fowler-Walker MJ, Connell SD (2002) Opposing states of subtidal habitat across temperate Australia: consistency and predictability in kelp canopy-benthic associations. Mar Ecol Prog Ser 240:49–56CrossRefGoogle Scholar
  18. Friedmann I (1969) Geographic and environmental factors controlling life history and morphology in Prasiola stipitata Suhr. Osterr Bot Z 116:203–225CrossRefGoogle Scholar
  19. Glanz SA, Slinker B (1990) Primer of applied regression and analysis of variance. McGraw-Hill, New YorkGoogle Scholar
  20. Haring RN, Dethier MN, Williams SL (2002) Desiccation facilitates wave-induced mortality of the intertidal alga, Fucus gardneri. Mar Ecol Prog Ser 232:75–82CrossRefGoogle Scholar
  21. Harley CDG (2003) Abiotic stress and herbivory interact to set range limits across a two-dimensional stress gradient. Ecology 84:1477–1488CrossRefGoogle Scholar
  22. Harley CDG, Helmuth BST (2003) Local- and regional-scale effects of wave exposure, thermal stress, and absolute versus effective shore level on patterns of intertidal zonation. Limnol Oceanogr 48:1498–1508CrossRefGoogle Scholar
  23. Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241CrossRefGoogle Scholar
  24. Hawkins SJ, Hartnoll RG (1985) Factors determining the upper limits of intertidal canopy-forming algae. Mar Ecol Prog Ser 20:265–271CrossRefGoogle Scholar
  25. Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites, 2E. Academic Press, New York, pp 371–413CrossRefGoogle Scholar
  26. Hays CG (2007) Adaptive phenotypic differentiation across the intertidal gradient in the alga Silvetia compressa. Ecol 88:149–157CrossRefGoogle Scholar
  27. Helmuth B, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol Bull 201:374–384CrossRefGoogle Scholar
  28. Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology, and climate change: does mechanism matter? Annu Rev Physiol 67:177–201CrossRefGoogle Scholar
  29. Hemmi A, Makinen A, Jormalainen V, Honkanen T (2005) Responses of growth and phlorotannins in Fucus vesiculosus to nutrient enrichment and herbivory. Aquat Ecol 39:201–211CrossRefGoogle Scholar
  30. Horner RA, Garrison DL, Plumbley FG (1997) Harmful algal blooms and red tide problems on the U.S. west coast. Limnol Oceanogr 42:1076–1088CrossRefGoogle Scholar
  31. Ilvessalo H, Tuomi J (1989) Nutrient availability and accumulation of phenolic compounds in the brown alga Fucus vesiculosus. Mar Biol 101:115–119CrossRefGoogle Scholar
  32. Jonsson PR, Granhag L, Moschella PS, Åberg P, Hawkins SJ, Thompson RC (2006) Interactions between wave action and grazing control the distribution of intertidal macroalgae. Ecology 87:1169–1178CrossRefGoogle Scholar
  33. Jormalainen V, Honkanen T, Koivikko R, Eränen J (2003) Induction of plorotannin production in a brown alga: defense or resource dynamics? Oikos 103:640–650CrossRefGoogle Scholar
  34. Keser M, Swenarton JT, Foertch JF (2005) Effects of thermal input and climate change on growth of Ascophyllum nodosum (Fucales, Phaeophyceae) in eastern Long Island Sound (USA). J Sea Res 54:211–220CrossRefGoogle Scholar
  35. Lambert M, Neish AC (1950) Rapid method for the estimation of glycerol in fermentation solutions. Can J Res 28:80–88Google Scholar
  36. Lehvo A, Bäck J, Kiirikki M (2001) Growth of Fucus vesiculosus L. (Phaeophyta) in the northern Baltic proper: energy and nitrogen storage in seasonal environment. Bot Mar 44:345–350CrossRefGoogle Scholar
  37. Leigh EG Jr, Paine RT, Quinn JF, Suchanek TH (1987) Wave energy and intertidal productivity. Proc Natl Acad Sci USA 84:1314–1318CrossRefGoogle Scholar
  38. Lubchenco J (1980) Algal zonation in the New England rocky intertidal community: an experimental analysis. Ecology 61:333–344CrossRefGoogle Scholar
  39. Lüning K (1993) Environmental and internal control of seasonal growth in seaweeds. Hydrobiologia 260(261):1–14CrossRefGoogle Scholar
  40. Malta E, Verschuure JM (1997) Effects of environmental variables on between-year variation of Ulva growth and biomass in a eutrophic brackish lake. J Sea Res 38:71–84CrossRefGoogle Scholar
  41. Mann KH (1982) Ecology of coastal waters: a systems approach. University of California Press, BerkeleyGoogle Scholar
  42. Mathieson AC, Shipman JW, O’Shea JR, Hasevlat RC (1976) Seasonal growth and reproduction of estuarine fucoid algae in New England. J Exp Mar Biol Ecol 25:273–284CrossRefGoogle Scholar
  43. Middleboe AL, Sand-Jensen K, Binzer T (2006) Highly predictable photosynthetic production in natural macroalgal communities from incoming and absorbed light. Oecologia 150:464–476CrossRefGoogle Scholar
  44. Niemeck RA, Mathieson AC (1976) An ecological study of Fucus spiralis L. J Exp Mar Biol Ecol 24:33–48CrossRefGoogle Scholar
  45. Pavia H, Toth G, Åberg P (1999) Trade-offs between phlorotannin production and annual growth in natural populations of the brown seaweed Ascophyllum nodosum. J Ecol 87:761–771CrossRefGoogle Scholar
  46. Renaud PE, Hay ME, Schmitt TM (1990) Interactions of plant stress and herbivory: intraspecific variation in the susceptibility of a palatable versus an unpalatable seaweed to sea urchin grazing. Oecologia 82:217–226CrossRefGoogle Scholar
  47. Rico JM (1991) Field studies and growth experiments on Gelidium latifolium from Asturias (northern Spain). Hydrobiologia 22:67–75CrossRefGoogle Scholar
  48. Santos R (1993) A multivariate study of biotic and abiotic relationships in a subtidal algal stand. Mar Ecol Prog Ser 94:181–190CrossRefGoogle Scholar
  49. SAS (2004) SAS 9.1 procedures guide. SAS Institute, Inc, CaryGoogle Scholar
  50. Schonbeck MW, Norton TA (1980) Factors controlling the lower limits of fucoid algae on the shore. J Exp Mar Biol Ecol 43:131–150CrossRefGoogle Scholar
  51. Scrosati R, Heaven C (2007) Spatial trends in community richness, diversity, and evenness across rocky intertidal environmental stress gradients in eastern Canada. Mar Ecol Prog Ser 342:1–14CrossRefGoogle Scholar
  52. Stengel DB, Dring MJ (1997) Morphology and in situ growth rates of plants of Ascophyllum nodosum (Phaeophyta) from different shore levels and responses of plants to vertical transplantation. Eur J Phycol 32:193–202CrossRefGoogle Scholar
  53. Strömgren T (1977a) Length growth rates of three species of intertidal Fucales during exposure to air. Oikos 29:245–249CrossRefGoogle Scholar
  54. Strömgren T (1977b) Short-term effects of temperature upon the growth of intertidal Fucales. J Exp Mar Biol Ecol 29:181–195CrossRefGoogle Scholar
  55. Strömgren T (1983) Temperature-length growth strategies in the littoral algal Ascophyllum nodosum (L.). Limnol Oceanogr 28:516–521CrossRefGoogle Scholar
  56. Thom RM (1983) Spatial and temporal patterns of Fucus distichus ssp. edentatus (de la Pyl.) Pow. (Phaeophyceae: Fucales) in Central Puget Sound. Bot Mar 26:471–486CrossRefGoogle Scholar
  57. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeGoogle Scholar
  58. Valiela I (1984) Marine ecological processes. Springer, New YorkCrossRefGoogle Scholar
  59. Van Alstyne KL (1988) Herbivore grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69:655–663CrossRefGoogle Scholar
  60. Van Alstyne KL (1990) Effects of wounding by the herbivorous snails Littorina sitkana and L. scutulata (Mollusca) on growth and reproduction of the intertidal alga Fucus distichus (Phaeophyta). J Phycol 26:412–416CrossRefGoogle Scholar
  61. Williams SL, Dethier MN (2005) High and dry: variation in net photosynthesis of the intertidal seaweed, Fucus gardneri. Ecology 86:2375–2379Google Scholar
  62. Wolcott BD (2007) Mechanical size limitation and life-history strategy of an intertidal seaweed. Mar Ecol Prog Ser 338:1–10CrossRefGoogle Scholar
  63. Wright JT, Williams SL, Dethier MN (2004) No zone is always greener: Fucus gardneri embryos, juveniles and adults are differentially affected by season and zone. Mar Biol 145:1061–1073CrossRefGoogle Scholar
  64. Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Department of Biology and Friday Harbor LabsUniversity of WashingtonFriday HarborUSA
  2. 2.Bodega Marine LaboratoryUniversity of California at DavisBodega BayUSA

Personalised recommendations