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Marine Biology

, 166:156 | Cite as

Assessing a macroalgal foundation species: community variation with shifting algal assemblages

  • Jacob R. MetzgerEmail author
  • Brenda Konar
  • Matthew S. Edwards
Original Paper

Abstract

Foundation species have strong, positive effects on local community structure; increasing biodiversity and species abundances by providing food and habitat. On coastal temperate and subpolar rocky reefs, canopy-forming kelps form three-dimensional habitats that support numerous fish, invertebrate, and algal species. Throughout the Aleutian Archipelago, unregulated sea urchin grazing has largely removed the foundation canopy-forming kelp, Eualaria fistulosa, and most subcanopy algae. Consequently, most nearshore rocky reefs have shifted from kelp to sea urchin (Strongylocentrotus spp.) dominated habitats. These latter habitats are either urchin barrens devoid of all fleshy macroalgae, or transition forests devoid of all fleshy macroalgae algae but E. fistulosa. These three distinct communities (kelp and transition forests, and urchin barrens) were used to test the influence of E. fistulosa and sea urchins on the associated communities. Contrary to initial expectations, in transition forest habitats where E. fistulosa is the lone macroalga, no differences in community structure or in the size structure of benthic invertebrates were seen relative to urchin barrens. In kelp forests, where E. fistulosa coexisted with subcanopy macroalgae and urchins were less abundant, faunal communities were more species rich with higher abundance, biomass, and percent cover of numerous filter feeders. These findings stress not only the strong negative impact which urchins can exert on the kelp forest communities, but also the context-dependent nature of foundation species.

Notes

Funding

This study was funded by the National Science Foundation (Award Number: 1435205).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study did use animals in the research protocols. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (University of Alaska Fairbanks Institutional Animal Care and Use Committee; Permit Number: 899401-4). For vertebrate animals, only field observations were conducted. For invertebrate collections, organisms were held in live tank prior to sampling and processed as expeditiously as possible before replacement to their home habitats. This study did not use human participants; therefore, informed consent was not applicable.

References

  1. Alongi DM (2002) Present state and future of the world’s mangrove forests. Environ Conserv 29:331–349Google Scholar
  2. Altieri AH, Silliman BR, Bertness MD (2007) Hierarchical organization via a facilitation cascade in intertidal cordgrass bed communities. Am Nat 169:195–206PubMedGoogle Scholar
  3. Andren H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different populations of suitable habitat: a review. Oikos 71:355–366Google Scholar
  4. Anthony RG, Estes JA, Ricca MA, Miles AK, Forsman ED (2008) Bald eagles and sea otters in the Aleutian Archipelago: indirect effects of trophic cascades. Ecology 89:2725–2735PubMedGoogle Scholar
  5. Araújo RM, Assis J, Aguillar R, Airoldi L, Bárbara I, Bartsch I, Bekkby T, Christie H, Davoult D, Derrien-Courtel S, Fernandez C, Fredriksen S, Gevaert F, Gundersen H, Le Gal A, Lévêque L, Mieszkowska N, Norderhaug KM, Oliveira P, Puente A, Rico JM, Rinde E, Schubert H, Strain EM, Valero M, Viard F, Sousa-Pinto I (2016) Status, trends and drivers of kelp forests in Europe: an expert assessment. Biodivers Conserv 25:1319–1348Google Scholar
  6. Arkema KK, Reed DC, Schroeter SC, Katie K, Reed DC, Schroeter SC (2017) Direct and indirect effects of giant kelp determine benthic community structure and dynamics. Ecology 90:3126–3137Google Scholar
  7. Bender DJ, Contreras TA, Fahrig L (1998) Habitat loss and population decline: a meta-analysis of the patch size effect. Ecology 79:517–533Google Scholar
  8. Bruno J, Bertness MD (2001) Positive interactions, facilitations and foundation species. Mar Commun Ecol Sinauer Assoc Inc Publ Sunderland, Massachusetts 201–218Google Scholar
  9. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125Google Scholar
  10. Carr MH (1994) Effects of macroalgal dynamics on recruitment of temperate reef fish. Ecology 75:1320–1333Google Scholar
  11. Cavanaugh KC, Siegel DA, Kinlan BP, Reed DC (2010) Scaling giant kelp field measurements to regional scales using satellite observations. Mar Ecol Prog Ser 403:13–27Google Scholar
  12. Christie H, Norderhaug KM, Fredriksen S (2009) Macrophytes as habitat for fauna. Mar Ecol Prog Ser 396:221–233Google Scholar
  13. Cie D, Edwards M (2011) Vertical distribution of kelp zoospores. Phycologia 50:340–350Google Scholar
  14. Clark RP, Edwards MS, Foster MS (2004) Effects of shade from multiple kelp canopies on an understory algal assemblage. Mar Ecol Prog Ser 267:107–119Google Scholar
  15. Clarke K, Gorley R (2015) PRIMER v7: user manual/tutorial. Plymouth Marine Laboratory, PlymouthGoogle Scholar
  16. Cole VJ, McQuaid CD (2010) Bioengineers and their associated fauna respond differently to the effects of biogeography and upwelling. Ecology 91:3549–3562PubMedGoogle Scholar
  17. Dayton PK (1972) Toward an understanding of community resilience and the potential effects of enrichment to the benthos at McMurdo Sound, Antarctica. Proceeding of the colloquium on conservation problems in Antarctica. Allen Press, Lawrence, pp 81–96Google Scholar
  18. Deza AA, Anderson TW (2010) Habitat fragmentation, patch size, and the recruitment and abundance of kelp forest fishes. Mar Ecol Prog Ser 416:229–240Google Scholar
  19. Doroff AM, Estes JA, Tinker MT, Burn DM, Evans TJ (2003) Sea otter population declines in the Aleutian Archipelago. J Mammal 84:55–64Google Scholar
  20. Drew EA (1983) Physiology of Laminaria. Mar Ecol 4:227–250Google Scholar
  21. Eckman JE, Duggins DO (1991) Life and death beneath macrophyte canopies: effects of understory kelps on growth rates and survival of marine, benthic suspension feeders. Oecologia 87:473–487PubMedGoogle Scholar
  22. Eckman JE, Duggins DO, Sewell AT (1989) Ecology of under story kelp environments. I. Effects of kelps on flow and particle transport near the bottom. J Exp Mar Bio Ecol 129:173–187Google Scholar
  23. Efird TP, Konar B (2014) Habitat characteristics can influence fish assemblages in high latitude kelp forests. Environ Biol Fishes 97:1253–1263Google Scholar
  24. Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel BD, Knoepp JD, Lovett GM, Mohan J, Orwig DA, Rodenhouse NL, Sobczak WV, Stinson KA, Stone JK, Swan CM, Thompson J, Von Holle B, Webster JR (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486Google Scholar
  25. Estes JA, Duggins DO (1995) Sea otters and kelp forests in Alaska: generality and variation in a community ecological paradigm. Ecol Monogr 65:75–100Google Scholar
  26. Estes JA, Palmisano JF (1974) Sea otters: their role in structuring nearshore communities. Science 185:1058–1060PubMedGoogle Scholar
  27. Estes JA, Smith NS, Palmisano JF (1978) Sea otter predation and community organization in the Western Aleutian Islands, Alaska. Ecology 59:822–833Google Scholar
  28. Estes JA, Tinker MT, Williams TM, Doak DF (1998) Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282:473–476PubMedGoogle Scholar
  29. Estes JA, Tinker MT, Bodkin JL (2010) Using ecological function to develop recovery criteria for depleted species: sea otters and kelp forests in the Aleutian Archipelago. Conserv Biol 24:852–860PubMedGoogle Scholar
  30. Field P, Dieckmann NG, Velimirov CL (1977) Sun, waves, seaweed and lobsters: the dynamics of a west coast kelp-bed. S Afr J Sci 73:7Google Scholar
  31. Filbee-Dexter K, Scheibling R (2014) Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar Ecol Prog Ser 495:1–25Google Scholar
  32. Fraser CI, Nikula R, Waters JM (2011) Oceanic rafting by a coastal community. Proc R Soc B 278:649–655PubMedGoogle Scholar
  33. Gaylord B, Hill TM, Sanford E, Lenz EA, Jacobs LA, Sato KN, Russell AD, Hettinger A (2011) Functional impacts of ocean acidification in an ecologically critical foundation species. J Exp Biol 214:2586–2594PubMedGoogle Scholar
  34. Gili JM, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol Evol 13:316–321PubMedGoogle Scholar
  35. Goodsell PJ, Fowler-Walker MJ, Gillanders BM, Connell SD (2004) Variations in the configuration of algae in subtidal forests: implications for invertebrate assemblages. Austral Ecol 29:350–357Google Scholar
  36. Graham MH (2004) Effects of local deforestation on the diversity and structure of Southern California Giant kelp forest food webs. Ecosystems 7:341–357Google Scholar
  37. Graham MH, Fox MD, Hamilton SL (2013) Macrophyte productivity and the provisioning of energy and habitat to nearshore systems. Mar Macrophytes as Found species 133–160Google Scholar
  38. Gribben PE, Byers JE, Clements M, McKenzie LA, Steinberg PD, Wright JT (2009) Behavioral interactions between ecosystem engineers control community species richness. Ecol Lett 12:1127–1136PubMedGoogle Scholar
  39. Gribben PE, Kimbro DL, Verges A, Gouhier TC, Burrel S, Garthwin RG, Cagigas ML, Tordoff Y, Poore AGB (2017) Positive and negative interactions control a facilitation cascade. Ecol Lett 8:1127–1136Google Scholar
  40. Himmelman JH, Steele DH (1971) Foods and predators of the green sea urchin Strongylocentrotus droebachiensis in Newfoundland waters. Mar Biol 9:315–322Google Scholar
  41. Hondolero D, Edwards MS (2017) Physical and biological characteristics of kelp forests in Kachemak Bay, Alaska. Mar Bio 164:81–93Google Scholar
  42. Hughes BB (2010) Variable effects of a kelp foundation species on rocky intertidal diversity and species interactions in central California. J Exp Mar Bio Ecol 393:90–99Google Scholar
  43. Hunt GL, Stabeno PJ (2005) Oceanography and ecology of the Aleutian Archipelago: spatial and temporal variation. Fish Oceanogr 14:292–306Google Scholar
  44. Irons DB, Anthony RG, Estes JA (2016) Foraging strategies of glaucous-winged gulls in a rocky intertidal community. Ecology 67:1460–1474Google Scholar
  45. Jackson GA (1977) Nutrients and production of giant kelp, Macrocystis pyrifera, off Southern California. Limnol Oceanogr 22:979–995Google Scholar
  46. Jangoux M, Lawrence J (1982) Echinoderm nutrition. CRC Press, Boca RatonGoogle Scholar
  47. Jensen J, Estes JA, Tinney L (1980) Remote-sensing techniques for kelp surveys. Photogramm Eng Remote Sens 46:743–755Google Scholar
  48. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386Google Scholar
  49. Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957Google Scholar
  50. Kirkman H (1984) Standing stock and production of Ecklonia radiata (C. Ag.). J Agardh J Exp Mar Bio Ecol 76:119–130Google Scholar
  51. Knip DM, Scheibling RE (2007) Invertebrate fauna associated with kelp enhances reproductive output of the green sea urchin Strongylocentrotus droebachiensis. J Exp Mar Bio Ecol 351:150–159Google Scholar
  52. Knowlton N, Jackson JBC (2001) The ecology of coral reefs. Mar Commun Ecol 395–422Google Scholar
  53. Konar B (2000a) Limited effects of a keystone species: trends of sea otters and kelp forests at the Semichi Islands, Alaska. Mar Ecol Prog Ser 199:271–280Google Scholar
  54. Konar B (2000b) Seasonal inhibitory effects of marine plants on sea urchins: structuring communities the algal way. Oecologia 125:208–217PubMedGoogle Scholar
  55. Konar B, Edwards MS, Estes JA (2014) Biological interactions maintain the boundaries between kelp forests and urchin barrens in the Aleutian Archipelago. Hydrobiologia 724:91–107Google Scholar
  56. Konar B, Edwards MS, Efird T (2015) Local habitat and regional oceanographic influence on fish distribution patterns in the diminishing kelp forests across the Aleutian Archipelago. Environ Biol Fishes 98:1935–1951Google Scholar
  57. Konar B, Edwards MS, Bland A, Metzger J, Ravelo A, Traiger S, Weitzman B (2017) A swath across the great divide: kelp forests across the Samalga Pass biogeographic break. Continent Shelf Res 143:78–88Google Scholar
  58. Larkum AWD (1986) A study of growth and primary production in Ecklonia radiata (C. Ag.) J. Agardh (Laminariales) at a sheltered site in Port Jackson, New South Wales. J Exp Mar Bio Ecol 96:177–190Google Scholar
  59. Laurance WF, Nascimento HEM, Laurance SG, Andrade A, Ewers RM, Harms KE, Luizão RCC, Ribeiro JE (2007) Habitat fragmentation, variable edge effects, and the landscape-divergence hypothesis. PLoS ONE.  https://doi.org/10.1371/journal.pone.0001017 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Lauzon-Guay JS, Scheibling RE, Barbeau MA (2009) Modelling phase shifts in a rocky subtidal ecosystem. Mar Ecol Prog Ser 375:25–39Google Scholar
  61. Lawrence JM (1975) On the relationships between marine plants and sea urchins. Oceanogr Mar Biol An Annu Rev 13:213–286Google Scholar
  62. Ling SD, Johnson CR, Frusher SD, Ridgway KR (2009) Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proc Natl Acad Sci USA 106:22341–22345PubMedGoogle Scholar
  63. Ling SD, Scheibling RE, Rassweiler A, Johnson CR, Shears N, Connell SD, Salomon AK, Norderhaug KM, Perez-Matus A, Hernandez JC, Clemente S, Blamey LK, Hereu B, Ballesteros E, Sala E, Garrabou J, Cebrian E, Zabala M, Fujita D, Johnson LE (2014) Global regime shift dynamics of catastrophic sea urchin overgrazing. Philos Trans R Soc B 370:20130269Google Scholar
  64. Mann KH (1973) Seaweeds: their productivity and strategy for growth. Science 182:975–981PubMedGoogle Scholar
  65. Marzinelli EM, Leong MR, Campbell AH, Steinberg PD, Verges A (2016) Does restoration of a habitat-forming seaweed restore associated faunal diversity? Rest Ecol 24:81–90Google Scholar
  66. Minor MA, Scheibling RE (1997) Effects of food ration and feeding regime on growth and reproduction of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 129:159–167Google Scholar
  67. O’Clair RM, Lindstrom SC (2000) North Pacific Seaweeds. Plant Press, Auke BayGoogle Scholar
  68. Ostroumov SA (2005) Some aspects of water filtering activity of filter-feeders. Hydrobiologia 542:275–286Google Scholar
  69. Peterson CH, Luettich RA, Micheli F, Skilleter GA (2004) Attenuation of water flow inside seagrass canopies of differing structure. Mar Ecol Prog Ser 268:81–92Google Scholar
  70. Pielou E (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131–144Google Scholar
  71. Reisewitz SE, Estes JA, Simenstad CA (2006) Indirect food web interactions: sea otters and kelp forest fishes in the Aleutian archipelago. Oecologia 146:623–631PubMedGoogle Scholar
  72. Rothäusler E, Gómez I, Hinojosa IA, Karsten U, Tala F, Thiel M (2009) Effect of temperature and grazing on growth and reproduction of floating Macrocystis spp. (phaeophyceae) along a latitudinal gradient. J Phycol 45:547–559PubMedGoogle Scholar
  73. Schuster M, Konar B (2014) Foliose algal assemblages and deforested barren areas: phlorotannin content, sea urchin grazing and holdfast community structure in the Aleutian dragon kelp, Eualaria fistulosa. Mar Biol 161:2319–2332Google Scholar
  74. Simenstad CA, Estes JA, Kenyon KW (1978) Aleuts, sea otters, and alternate stable-state communities. Science 200:403–411PubMedGoogle Scholar
  75. Smale DA, Burrows MT, Moore P, O’Connor N, Hawkins SJ (2013) Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecol Evol 3:4016–4038PubMedPubMedCentralGoogle Scholar
  76. Springer YP, Hays CG, Carr MH, Mackey MR (2010) Toward ecosystem-based management of marine macroalgae—the bull kelp, Nereocystis luetkeana. Oceanogr Mar Biol 48:1–42Google Scholar
  77. Spyksma AJP, Taylor RB, Shears NT (2017) Predation cues rather than resource availability promote cryptic behaviour in a habitat-forming sea urchin. Oecologia 183:821–829PubMedGoogle Scholar
  78. Stachowicz JJ (2001) Mutualism, facilitation, and structure of ecological communities. Bioscience 51:235–246Google Scholar
  79. Stadniczeñko SG, Pedersen MF, Christie H, Fredriksen S, Norderhaug KM (2015) Population dynamics of Strongylocentrotus droebachiensis in kelp forests and barren grounds in Norway. Mar Biol 162:1215–1226Google Scholar
  80. Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459Google Scholar
  81. Stewart NL, Konar B (2012) Kelp forest versus urchin barrens: alternate stable states and their effect on sea otter prey quality in the Aleutian Islands. J Mar Bio.  https://doi.org/10.1155/2012/492308 CrossRefGoogle Scholar
  82. U.S. Fish and Wildlife Service (2013) Southwest Alaska DPS of the Northern Sea Otter (Enhydra lutris kenyoni) 5-Year Review: summary and evaluation. Anchorage, AKGoogle Scholar
  83. Vicknair K, Estes JA (2012) Interactions among sea otters, sea stars, and suspension-feeding invertebrates in the western Aleutian archipelago. Mar Biol 159:2641–2649Google Scholar
  84. Warwick RM, Clarke KR (1995) New biodiversity measures reveal a decrease in taxonomic distinctiveness with increasing stress. Mar Ecol Prog Ser 301–305Google Scholar
  85. Watson J, Estes JA (2011) Stability, resilience, and phase shifts in rocky subtidal communities along the west coast of Vancouver Island, Canada. Ecol Monogr 81:215–239Google Scholar
  86. Yakovis EL, Artemieva AV, Shunatova NN, Varfolomeeva MA (2008) Multiple foundation species shape benthic habitat islands. Oecologia 155:785–795PubMedGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.University of Alaska FairbanksFairbanksUSA
  2. 2.Department of BiologySan Diego State UniversitySan DiegoUSA

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