Skip to main content
Log in

Accelerating Trophic-level Dysfunction in Kelp Forest Ecosystems of the Western North Atlantic

  • Special Feature
  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

We use archaeological, historical, ecological, and fisheries data to identify three distinct and sequential phases in the trophic structure of kelp forests in the western North Atlantic’s Gulf of Maine. Phase 1 is characterized by vertebrate apex predators such as Atlantic cod, haddock, and wolffish and persisted for more than 4,000 years. Phase 2 is characterized by herbivorous sea urchins and lasted from the 1970s to the 1990s. Phase 3 is dominated by invertebrate predators such as large crabs and has developed since 1995. Each phase change resulted directly or indirectly from fisheries-induced “trophic-level dysfunction,” in which populations of functionally important species at higher trophic levels fell below the densities necessary to limit prey populations at lower trophic levels. By using fractional trophic-level analysis, we found that phase changes occurred rapidly (over a few years to a few decades) as well as relatively recently (over the past half-century). Interphase durations have declined as fishing effects have accelerated in recent years. The naturally low species diversity of the kelp forest ecosystem we studied may facilitate rapid changes because the redundancy within each trophic level is low. If the biodiversity within controlling trophic levels is a buffer against trophic-level dysfunction, then our observations from Maine may be predictive of the fate of other, more diverse systems. If fishing successively targets most, or all, strong interactors at higher trophic levels, then as those population densities decline, the potential for trophic-level dysfunction and associated instabilities will increase.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1.
Figure 2.

Similar content being viewed by others

References

  1. WH Adey RS Steneck (2001) ArticleTitleThermogeography over time creates biogeographic regions: a temperature/space/time-integrated model and an abundance-weighted test for benthic marine algae J Phycol 37 677–98 Occurrence Handle10.1046/j.1529-8817.2001.00176.x

    Article  Google Scholar 

  2. MP Austin BG Cook (1974) ArticleTitleEcosystem stability: a result from an abstract simulation J Theoret Biol 45 435–58 Occurrence Handle1:STN:280:CSuB1c7lsVI%3D

    CAS  Google Scholar 

  3. HB Bigelow WC Schroeder (1953) ArticleTitleFishes of the Gulf of Maine Fish Bull 53 1–577

    Google Scholar 

  4. BJ Bourque (1995) Diversity and complexity in prehistoric maritime societies: a Gulf of Maine perspective Plenum Press New York

    Google Scholar 

  5. BJ Bourque (2001) Twelve thousand years: American Native Americans in Maine University of Nebraska Press Lincoln (NE) 368

    Google Scholar 

  6. PA Breen KH Mann (1976) ArticleTitleChanging lobster abundance and the destruction of kelp beds by sea urchins Mar Biol 34 137–42

    Google Scholar 

  7. Carlson CC. 1986. Maritime catchment areas: an analysis of prehistoric fishing strategies in the Boothbay region of Maine [thesis]. Orono (ME): University of Maine.

  8. Chapman, ARO (1981) “Stability of sea urchin dominated barrengrounds following destructive grazing of Kelp in St. Margaret’s Bay, Eastern Canada” Mar. Biol. 62: 307–311

    Google Scholar 

  9. ARO Chapman (1984) ArticleTitleReproduction, recruitment and mortality in two species of Laminaria in southwest Nova Scotia J Exp Mar Biol Ecol 78 99–109 Occurrence Handle10.1016/0022-0981(84)90072-8

    Article  Google Scholar 

  10. ARO Chapman (1986) ArticleTitleAge vs. stage an analysis of age-specific and size-specific mortality and reproduction in a population of Laminaria longicruris J Exp Mar Biol Ecol 97 113–22 Occurrence Handle10.1016/0022-0981(86)90113-9

    Article  Google Scholar 

  11. JW Collins R Rathbun (1887) Fishing grounds of the eastern coast of North America GB Goode (Eds) The fisheries and fishing industries of the U.S. Section III US Government Printing Office Washington (DC) 247–313

    Google Scholar 

  12. PW Conkling T Ames (1996) Fishing grounds of the eastern coast of North America DD Platt (Eds) Penobscot: the forest, river and bay Island Institute Rockland (ME) 46–65

    Google Scholar 

  13. JH Connell WP Sousa (1983) ArticleTitleOn the evidence needed to judge ecological stability or persistence Am Nat 121 789–824 Occurrence Handle10.1086/284105

    Article  Google Scholar 

  14. PK Dayton (1975) ArticleTitleExperimental studies of algal canopy interactions in sea otter–dominated kelp community at Amchitka Island, Alaska Fish Bull 73 230–7

    Google Scholar 

  15. [DMR] Department of Marine Resources (ME). 1971–2000. Maine fisheries landings. Augusta (ME): Department of Marine Resources.

  16. JM Erlandson TC Rick RL Vellanoweth (2004) Human impacts on ancient environments: a case study from California’s northern Channel Islands SM Fitzpatrick (Eds) Voyages of discovery: examining the past in island environments Praeger New York 51–83

    Google Scholar 

  17. JA Estes DO Duggins GB Rathbun (1989) ArticleTitleThe ecology of extinctions in kelp forest communities Conserv Biol 3 252–64

    Google Scholar 

  18. Froese R, Pauly D, editors. 2002. FishBase. Available online at: www.fishbase.org, 20 September 2002.

  19. Gilbert JR, Guldager N. 1998. Status of harbor and gray seal populations in northern New England. Woods Hole (MA): National Marine Fisheries Service.

  20. SD Hacker RS Steneck (1990) ArticleTitleHabitat architecture and the abundance and body-size-dependent habitat selection of a phytal amphipod Ecology 71 2269–85

    Google Scholar 

  21. NG Hairston FE Smith LB Slobodkin (1960) ArticleTitleCommunity structure, population control, and competition Am Nat 94 421–5 Occurrence Handle10.1086/282146

    Article  Google Scholar 

  22. NG Hairston JD Allan RK Colwell DJ Futuyama J Howell MD Lubin J Mathias et al. (1968) ArticleTitleThe relationship between species diversity and stability: an experimental approach with protozoa and bacteria Ecology 49 1091–101

    Google Scholar 

  23. C Harrold DC Reed (1985) ArticleTitleFood availability, sea urchin grazing, and kelp forest community structure Ecology 66 1160–9

    Google Scholar 

  24. AB Hervey (1881) Sea mosses: a collector’s guide and an introduction to the study of marine algae SE Cassino Salem (MA)

    Google Scholar 

  25. JBC Jackson MX Kirby WH Berger KA Bjorndal LW Botsford BJ Bourque RH Bradbury et al. (2001) ArticleTitleHistorical overfishing and the recent collapse of coastal ecosystems Science 293 629–38 Occurrence Handle10.1126/science.1063789 Occurrence Handle1:CAS:528:DC%2BD3MXls1Khu7o%3D Occurrence Handle11474098

    Article  CAS  PubMed  Google Scholar 

  26. DS Johnson AF Skutch (1928) ArticleTitleLittoral vegetation on a headland of Mt. Desert Island, Maine. I. Submersible or strictly littoral vegetation Ecology 9 188–215

    Google Scholar 

  27. DW Keats DH Steele GR South (1986) ArticleTitleAtlantic wolffish (Anarhichas lupus L.; Pisces: Anarhichidae) predation on green sea urchins (Strongylocentrotus droebachiensis (O.F. Mull.); Echinodermata: Echinoidea) in eastern Newfoundland Can J Zool 64 1920–5

    Google Scholar 

  28. SJ Kennelly (1989) ArticleTitleEffects of kelp canopies on understory species due to shade and scour Mar Ecol Progr Ser 50 215–24

    Google Scholar 

  29. N Knowlton (1992) ArticleTitleThresholds and multiple stable states in coral reef community dynamics Am Zool 32 674–82

    Google Scholar 

  30. B Konar (2000) ArticleTitleSeasonal inhibitory effects of marine plants on sea urchins: structuring communities the algal way Oecologia 125 208–17 Occurrence Handle10.1007/s004420000440

    Article  Google Scholar 

  31. B Konar JA Estes (2003) ArticleTitleThe stability of boundary regions between kelp beds and deforested areas Ecology 84 174–85

    Google Scholar 

  32. I Lamb M Zimmerman (1964) ArticleTitleMarine vegetation on Cape Anne, Essex County, Massachusetts Rhodora 66 217–54

    Google Scholar 

  33. Leland AV. 2002. A new apex predator in the Gulf of Maine: crabs (Cancer borealis) control benthic community structure [thesis]. Orono (ME): University of Maine.

  34. PS Levin (1994) ArticleTitleSmall-scale recruitment variation in a temperate fish: the roles of macrophytes and food supply Environ Biol Fish 40 271–81

    Google Scholar 

  35. PS Levin IA Coyer R Petrik TP Good (2002) ArticleTitleCommunity-wide effects of non- indigenous species on temperature rocky reefs Ecology 83 3182–93

    Google Scholar 

  36. LF Lowery JS Pearse (1973) ArticleTitleAbalones and sea urchins in an area inhabited by sea otters Mar Biol 23 213–9

    Google Scholar 

  37. C MacFarlane (1952) ArticleTitleA survey of certain seaweeds of commercial importance in southwest Nova Scotia Can J Bot 30 78–97

    Google Scholar 

  38. Malpass WJ. 1992. The ecology and resource use patterns of small, benthic, predatory fishes in rocky nearshore habitats in the Gulf of Maine [thesis]. Orono (ME): University of Maine.

  39. RM May (1977) ArticleTitleThresholds and breakpoints in ecosystems with a multiplicity of stable states Nature 269 471–7

    Google Scholar 

  40. J McGrady-Steed PJ Morin (2000) ArticleTitleBiodiversity, density compensation, and the dynamics of populations and functional groups Ecology 81 361–73

    Google Scholar 

  41. McNaught DC. 1999. The indirect effects of macroalgae and micropredation on the post-settlement success of the green sea urchin in Maine [dissertation]. Orono (ME): University of Maine.

  42. S Naeem LJ Thompson SP Lawler JH Lawton RM Woodfin (1994) ArticleTitleDeclining biodiversity can alter the performance of ecosystems Nature 368 734–7 Occurrence Handle10.1038/368734a0

    Article  Google Scholar 

  43. A-M Neutal JAP Heesterbeek PC de Ruiter (2002) ArticleTitleStability in real food webs: weak links in long loops Science 296 1120–3 Occurrence Handle10.1126/science.1068326 Occurrence Handle12004131

    Article  PubMed  Google Scholar 

  44. [NMFS] National Marine Fisheries Service (US). 1971–2000. Fisheries of the United States. Washington (DC): US Government Printing Office.

  45. I Novaczek J McLachlan (1986) ArticleTitleRecolonization by algae of the sublittoral habitat of Halifax County, Nova Scotia, following the demise of sea urchins Bot Mar 29 69–73

    Google Scholar 

  46. RT Paine (1966) ArticleTitleFood web complexity and species diversity Am Nat 100 65–75 Occurrence Handle10.1086/282400

    Article  Google Scholar 

  47. RT Paine (1980) ArticleTitleFood webs: linkage, interaction strength and community infrastructure J Animal Ecol 49 667–85

    Google Scholar 

  48. D Pauly V Christensen J Dalsgaard R Froese F Torres Jr (1998) ArticleTitleFishing down marine food webs Science 279 860–3 Occurrence Handle10.1126/science.279.5352.860 Occurrence Handle1:CAS:528:DyaK1cXhtVOjtro%3D Occurrence Handle9452385

    Article  CAS  PubMed  Google Scholar 

  49. D Pauly R Palomares P Froese M Sa-a D Vakily S Preikshot D Wallace (2001) ArticleTitleFishing down Canadian aquatic food webs Can J Fish Aquat Sci 58 1–12 Occurrence Handle10.1139/cjfas-58-1-51

    Article  Google Scholar 

  50. D Pauly V Christensen S Guénette TJ Pitcher UR Sumaila CJ Walters R Watson et al. (2002) ArticleTitleTowards sustainability in world fisheries Nature 418 689–95 Occurrence Handle10.1038/nature01017 Occurrence Handle1:CAS:528:DC%2BD38XlvVyltbg%3D Occurrence Handle12167876

    Article  CAS  PubMed  Google Scholar 

  51. PS Petraitis RE Latham (1999) ArticleTitleThe importance of scale in testing the origins of alternative community states Ecology 80 429–42

    Google Scholar 

  52. GA Polis DR Strong (1996) ArticleTitleFood web complexity and community dynamics Am Nat 147 813–46 Occurrence Handle10.1086/285880

    Article  Google Scholar 

  53. Rich WH. 1929. Fishing grounds of the Gulf of Maine. Bureau of Fisheries Document 1959. p 51–117. US Government Printing Office, Washington D.C.

  54. J Rosier (1605) The true relations of Capt. George Weymouth’s voyage George Bishop London

    Google Scholar 

  55. E Sala M Graham (2002) ArticleTitleCommunity-wide distribution of predator–prey interaction strength in kelp forests Proc Natl Acad Sci US 99 3678–83 Occurrence Handle10.1073/pnas.052028499 Occurrence Handle1:CAS:528:DC%2BD38Xis1Klsbk%3D Occurrence Handle11891292

    Article  CAS  PubMed  Google Scholar 

  56. E Sala CF Bourdouresque M Harmelin-Vivien (1998) ArticleTitleFishing, trophic cascades, and the structure of algal assemblages: evaluation of an old but untested paradigm Oikos 82 425–39

    Google Scholar 

  57. M Scheffer S Carpenter JA Foley C Folke B Walker (2001) ArticleTitleCatastrophic shifts in ecosystems Nature 413 591–6 Occurrence Handle10.1038/35098000 Occurrence Handle1:CAS:528:DC%2BD3MXnsleht7c%3D Occurrence Handle11595939

    Article  CAS  PubMed  Google Scholar 

  58. RE Scheibling BG Hatcher (2001) The ecology of Strongylocentrotus droebachiensis JM Lawrence (Eds) Edible sea urchins Elsevier. Sci Netherlands 271–306

    Google Scholar 

  59. CA Simenstad JA Estes KW Kenyon (1978) ArticleTitleAleut, sea otters, and alternate stable state communities Science 200 403–411

    Google Scholar 

  60. J Smith (1616) The description of New England H. Lownes London

    Google Scholar 

  61. SI Smith (1879) ArticleTitleThe stalk-eyed crustaceans of the Atlantic coast of North America north of Cape Cod Trans Conn Acad 5 27–138

    Google Scholar 

  62. WP Sousa JH Connell (1985) ArticleTitleFurther comments on the evidence for multiple stable points in natural communities Am Nat 125 612–5 Occurrence Handle10.1086/284366

    Article  Google Scholar 

  63. AE Spiess R Lewis (2001) ArticleTitleThe Turner Farm fauna: five thousand years of hunting and fishing in Penobscot Bay, Maine Occ Publ Maine Archeol 11 1–120

    Google Scholar 

  64. RS Steneck (1982) ArticleTitleA limpet-coralline alga association: adaptations and defenses between a selective herbivore and its prey Ecology 63 507–22

    Google Scholar 

  65. RS Steneck (1997) Fisheries-induced biological changes to the structure and function of the Gulf of Maine ecosystem GT Wallace EF Braasch (Eds) Proceedings of the Gulf of Maine Ecosystem Dynamics Scientific Symposium and Workshop Regional Association for Research on the Gulf of Maine Hanover (NH) 151–65

    Google Scholar 

  66. RS Steneck (2001) Functional groups S Levin (Eds) Encyclopedia of biodiversity; vol 1 Academic Press New York 121–39

    Google Scholar 

  67. Steneck, RS, Carlton, JT (2001) bHuman alterations of marine communities: Students beware! In: Bertness, M., Gaines, S., Hay, M. (editors), Marine community Ecology, Sinaver Press, Sunderland, MA

  68. RS Steneck MN Dethier (1994) ArticleTitleA functional group approach to the structure of algal-dominated communities Oikos 69 476–98

    Google Scholar 

  69. RS Steneck MH Graham BJ Bourque D Corbett JM Erlandson JA Estes MJ Tegner (2003) ArticleTitleKelp forest ecosystems: biodiversity, stability, resilience and future Environ Conserv 29 436–59 Occurrence Handle10.1017/S0376892902000322

    Article  Google Scholar 

  70. D Tillman (1996) ArticleTitleBiodiversity: population versus ecosystem diversity Ecology 77 350–63

    Google Scholar 

  71. RL Vadas Sr BF Beal (1999) Temporal and spatial variability in the relationships between adult size, maturity and fecundity in green sea urchins: the potential use of a roe-yield standard as a conservation tool Maine Department of Marine Resources Augusta (ME)

    Google Scholar 

  72. RL Vadas Sr RS Steneck (1988) ArticleTitleZonation of deep water benthic algae in the Gulf of Maine J Phycol 24 338–46

    Google Scholar 

  73. RL Vadas Sr RS Steneck (1995) Overfishing and inferences in kelp–sea urchin interactions HR Skjoldal C Hopkins KE Erikstad HP Leinaas (Eds) Ecology of fjords and coastal waters Elsevier Netherlands 509–529

    Google Scholar 

  74. Vavrinec J. 2003. Resilience of green sea urchin (Strongylocentrotus droebachiensis) populations following fishing mortality: marine protected areas, larval ecology and post-settlement survival [dissertation]. Orono (ME): University of Maine.

  75. GJ Vermeij (1991) ArticleTitleAnatomy of an invasion: the trans-Arctic interchange Paleobiology 17 281–307

    Google Scholar 

  76. A Verrill (1871) ArticleTitleMarine fauna of Eastport, ME Bull Essex Inst 8 1–6

    Google Scholar 

  77. JD Witman (1985) ArticleTitleRefuges, biological disturbance, and rocky subtidal community structure in New England Ecol Monogr 55 421–45

    Google Scholar 

  78. JD Witman KP Sebens (1992) ArticleTitleRegional variation in fish predation intensity: a historical perspective in the Gulf of Maine Oecologia 90 305–15

    Google Scholar 

Download references

Acknowledgments

We thank Tim McClanahan for inviting us to write this paper and for his helpful critique. The research represented here has been funded by several sources, including the Pew Foundation for Marine Conservation, NOAA’s Sea Grant program to the University of Maine (to R.S.S.), Maine’s Department of Marine Resources (to R.S.S.), and the National Undersea Research Program’s National Research Center at the University of Connecticut at Avery Point (grants no. NA46RU0146 and UCAZP 94–121 to R.S.S.). Our colleagues shared insights and unpublished data for several kelp forest ecosystems worldwide and assisted us with analyses. In particular, we thank Susie Arnold, Chantale Bégin, Jim Estes, Michael Graham, Jeremy Jackson, Doug McNaught, Daniel Pauly, Bob Scheibling, Bob Vadas, our teams of summer interns, and two anonymous reviewers. To all we are grateful.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert S. Steneck.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Steneck, R., Vavrinec, J. & Leland, A. Accelerating Trophic-level Dysfunction in Kelp Forest Ecosystems of the Western North Atlantic. Ecosystems 7, 323–332 (2004). https://doi.org/10.1007/s10021-004-0240-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-004-0240-6

Navigation