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Trophic versus structural effects of a marine foundation species, giant kelp (Macrocystis pyrifera)

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Abstract

Foundation species create milieus in which ecosystems evolve, altering species abundances and distribution often to a dramatic degree. Although much descriptive work supports their importance, there remains little definitive information on the mechanisms by which foundation species alter their environment. These mechanisms fall into two basic categories: provision of food or other materials, and modification of the physical environment. Here, we manipulated the abundance of a marine foundation species, the giant kelp Macrocystis pyrifera, in 40 × 40-m plots at Mohawk Reef off Santa Barbara, California and found that its biomass had a strong positive effect on the abundance of bottom-dwelling sessile invertebrates. We examined the carbon (C) stable isotope values of seven species of sessile invertebrates in the treatment plots to test the hypothesis that this positive effect resulted from a nutritional supplement of small suspended particles of kelp detritus, as many studies have posited. We found no evidence from stable isotope analyses to support the hypothesis that kelp detritus is an important food source for sessile suspension-feeding invertebrates. The isotope composition of invertebrates varied with species and season, but was not affected by kelp biomass, with the exception of two species: the tunicate Styela montereyensis, which exhibited a slight enrichment in C stable isotope composition with increasing kelp biomass, and the hydroid Aglaophenia sp., which showed the opposite effect. These results suggest that modification of the physical habitat, rather than nutritional subsidy by kelp detritus, likely accounts for increased abundance of sessile invertebrates within giant kelp forests.

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References

  • Anderson TW (1994) Role of macroalgal structure in the distribution and abundance of a temperate reef fish. Mar Ecol Prog Ser 113:279–290

    Article  Google Scholar 

  • Anderson MJ, Millar RB (2004) Spatial variation and effects of habitat on temperate reef fish assemblages in northeastern New Zealand. J Exp Mar Biol Ecol 305:191–221

    Article  Google Scholar 

  • Andrew NL, Jones GP (1990) Patch formation by herbivorous fish in a temperate Australian kelp forest. Oecologia 85:57–68

    Article  Google Scholar 

  • Arkema KK, Reed DC, Schroeter SC (2009) Direct and indirect effects of giant kelp determine benthic community structure and dynamics. Ecology 90:3126–3137

    Article  PubMed  Google Scholar 

  • Box SJ, Mumby PJ (2007) Effect of macroalgal competition on growth and survival of juvenile Caribbean corals. Mar Ecol Prog Ser 342:139–149

    Article  Google Scholar 

  • Bruno JF, Bertness MD (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness MD, Hay ME, Gaines SD (eds) Marine community ecology. Sinauer, Sunderland, pp 201–218

    Google Scholar 

  • Bustamante RH, Branch GM (1996) The dependence of intertidal consumers on kelp-derived organic matter on the west coast of South Africa. J Exp Mar Biol Ecol 196:1–28

    Article  Google Scholar 

  • Butman CA, Grassle JP, Webb CM (1988) Substrate choices made by marine larvae settling in still water and in a flume flow. Nature 333:771–773

    Article  Google Scholar 

  • Byrnes JE, Reed DC, Cardinale BJ, Cavanaugh KC, Holbrook SJ, Schmitt RJ (2011) Climate driven increases in storm frequency simplify kelp forest food webs. Glob Chang Biol 17:2513–2524

    Article  Google Scholar 

  • Carr MH (1994) Effects of macroalgal dynamics on recruitment of a temperate reef fish. Ecology 75:1320–1333

    Article  Google Scholar 

  • Carr MH, Reed DC Shallow rocky reefs and kelp forests. In: Mooney H, Zavaleta E (eds) Ecosystems of California. University of California Press, Berkeley (in press)

  • Choat JH, Ayling AM (1987) The relationship between habitat structure and fish faunas on New Zealand reefs. J Exp Mar Biol Ecol 110:257–284

    Article  Google Scholar 

  • Christie H, Jørgensen NM, Norderhaug KM, Waage-Nielsen E (2003) Species distribution and habitat exploitation of fauna associated with kelp (Laminaria hyperborea) along the Norwegian coast. J Mar Biol Assoc UK 83:687–699

    Article  Google Scholar 

  • Cifuentes LA, Sharp JH, Fogel ML (1988) Stable carbon and nitrogen isotope biogeochemistry in the Delaware estuary. Limnol Oceanogr 33:1102–1115

    Article  CAS  Google Scholar 

  • Cohen J (2013) Statistical power analysis for the behavioral sciences. Routledge Academic, London

    Google Scholar 

  • Connell SD (2003) Negative effects overpower the positive of kelp to exclude invertebrates from the understorey community. Oecologia 137:97–103

    Article  PubMed  Google Scholar 

  • Dayton PK (1972) Toward an understanding of community resilience and the potential effects of enrichments to the benthos at McMurdo Sound, Antarctica. In: Parker BC (ed) Proceedings of the Colloquium on Conservation Problems in Antarctica. Allen Press, Lawrence

    Google Scholar 

  • Dayton PK (1985) Ecology of kelp communities. Annu Rev Ecol Syst 16:215–245

    Article  Google Scholar 

  • Dayton PK, Tegner MJ (1989) Bottoms beneath troubled waters: benthic impacts of the 1982–1984 El Nino in the temperate zone. In: Glynn PW (ed) Global ecological consequences of the 1982–83 El Nino-Southern Oscillation. Elsevier oceanography series no. 52. Elsevier, Amsterdam, pp 433–472

    Google Scholar 

  • Dayton PK, Tegner MJ, Edwards PB, Riser KL (1999) Temporal and spatial scales of kelp demography: the role of oceanographic climate. Ecol Monogr 69:219–250

    Article  Google Scholar 

  • Dugan JE, Hubbard DM, McCrary MD, Pierson MO (2003) The response of macrofauna communities and shorebirds to macrophyte wrack subsides on exposed sandy beaches of southern California. Estuar Coast Shelf Sci 58S:25–40

    Article  Google Scholar 

  • Duggins DO, Eckman JE (1994) The role of kelp detritus in the growth of benthic suspension feeders in an understory kelp forest. J Exp Mar Biol Ecol 176:53–68

    Article  Google Scholar 

  • Duggins DO, Eckman JE (1997) Is kelp detritus a good food for suspension feeders? Effects of kelp species, age and secondary metabolites. Mar Biol 128:489–495

    Article  Google Scholar 

  • Duggins DO, Simenstad CA, Estes JA (1989) Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245:170–173

    Article  CAS  PubMed  Google Scholar 

  • Dunton KH, Schell DM (1987) Dependence of consumers on macroalgal (Laminaria solidungula) carbon in an arctic kelp community: δ13C evidence. Mar Biol 93:615–625

    Article  CAS  Google Scholar 

  • Eckman JE, Duggins DO, Sewell AT (1989) Ecology of understory kelp environments. I. Effects of kelps on flow and particle transport near the bottom. J Exp Mar Biol Ecol 129:173–187

    Article  Google Scholar 

  • 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 3:479–486

    Article  Google Scholar 

  • Foster MS (1975) Regulation of algal community development in a Macrocystis pyrifera forest. Mar Biol 32:331–342

    Article  Google Scholar 

  • Fredriksen S (2003) Food web studies in a Norwegian kelp forest based on stable isotope (∆13C and ∆15N) analysis. Mar Ecol Prog Ser 260:71–81

    Article  CAS  Google Scholar 

  • Gaylord B, Reed DC, Washburn L, Raimondi PT (2004) Physical-biological coupling in spore dispersal of kelp forest macroalgae. J Mar Syst 49:19–39

    Article  Google Scholar 

  • Gaylord B, Rosman JH, Reed DC, Koseff JR, Fram J, MacIntyre S, Mardian B (2007) Spatial patterns of flow and their modification within and around a giant kelp forest. Limnol Oceanogr 52:1838–1852

    Article  Google Scholar 

  • Gerard VA 1976 Some aspects of material dynamics and energy flow in a kelp forest in Monterey Bay, California. Dissertation, University of California, Santa Cruz, CA

  • Gili JM, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends in Ecol and Evol 13:316–321

    Article  CAS  Google Scholar 

  • Gili JM, Hughes RG, Alvà V (1996) A quantitative study of feeding by the hydroid Tubularia larynx Ellis and Solander, 1786. Sci Mar 60:43–54

    Google Scholar 

  • Gotelli NJ (1987) Spatial and temporal patterns of reproduction, larval settlement, and recruitment of the compound ascidian Aplidium stellatum. Mar Biol 94:45–51

    Article  Google Scholar 

  • Graham MH (2004) Effects of local deforestation of the diversity and structure of southern California giant kelp forest food webs. Ecosystems 7:341–357

    Article  Google Scholar 

  • Graham MH, Vasquez JA, Buschmann AH (2007) Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. Ocean Mar Biol 45:39–88

    Google Scholar 

  • Harrold C, Reed DC (1985) Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66:1160–1169

    Article  Google Scholar 

  • Harrold C, Light K, Lisin S (1998) Organic enrichment of submarine-canyon and continental-shelf benthic communities by macroalgal drift imported from nearshore kelp forests. Limnol Oceanogr 43:669–678

    Article  Google Scholar 

  • Jackson GA (1998) Currents in the high drag environment of a coastal kelp stand off California. Cont Shelf Res 17:1913–1928

    Article  Google Scholar 

  • Jackson GA, Winant CD (1983) Effect of a kelp forest on coastal currents. Cont Shelf Res 2:75–80

    Article  Google Scholar 

  • Jones CG, Gutiérrez JL, Byers JE, Crooks JA, Lambrinos JG, Talley TS (2010) A framework for understanding physical ecosystem engineering by organisms. Oikos 119:1862–1869

    Article  Google Scholar 

  • Kaehler S, Pakhomov EA, McQuaid CD (2000) Trophic structure of the marine food web at the Prince Edward Islands (Southern Ocean) determined by δ13C and δ15N analysis. Mar Ecol Prog Ser 208:13–20

    Article  Google Scholar 

  • Kendrick GA, Harvey E, Wernberg T, Harman N, Goldberg N (2004) The role of disturbance in maintaining diversity of benthic macroalgal assemblages in southwestern Australia. Jpn J Phycol 52:5–9

    Google Scholar 

  • Klumpp DW (1984) Nutritional ecology of the ascidian Pyura stolonifera: influence of body size, food quantity and quality on filter-feeding, respiration, assimilation efficiency and energy balance. Mar Ecol Prog Ser 19:269–284

    Article  Google Scholar 

  • Krumhansl KA, Scheibling RE (2012) Production and fate of kelp detritus. Mar Ecol Prog Ser 467:281–302

    Article  Google Scholar 

  • Labarbera M (1984) Feeding currents and particle capture mechanisms in suspension feeding animals. Am Zool 24:71–84

    Article  Google Scholar 

  • Lafferty KD (2004) Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol Appl 14:1566–1573

    Article  Google Scholar 

  • Lastra M, Page HM, Dugan JE, Hubbard DM, Rodil I (2008) Processing of allochthonous macrophyte subsidies by sandy beach consumers: estimates of feeding rates and impacts on food resources. Mar Biol 154:163–174

    Article  Google Scholar 

  • Laws E, Popp B, Cassar N, Tanimoto J (2002) 13C discrimination patterns in oceanic phytoplankton: likely influence of CO2 concentrating mechanisms, and implications for palaeoreconstructions. Funct Plant Biol 29:323–333

    Article  CAS  Google Scholar 

  • Lewis SM (1986) The role of herbivorous fishes in the organization at a coral reef community. Ecol Monogr 56:183–200

    Article  Google Scholar 

  • Mann KH (1977) Destruction of kelp-beds by sea-urchins: a cyclical phenomenon or irreversible degradation? Helgol Meer 30:455–467

    Article  Google Scholar 

  • Mann K (1988) Production and use of detritus in various freshwater, estuarine, and coastal marine ecosytems. Limnol Oceanogr 33:910–930

    Article  CAS  Google Scholar 

  • Mattison JE, Trent JE, Shanks AL, Akin TB, Pearse JS (1977) Movement and feeding activity of red sea urchins (Strongylocentrotus franciscanus) adjacent to a kelp forest. Mar Biol 39:25–31

    Article  Google Scholar 

  • Miller RJ, Etter RJ (2008) Shading facilitates sessile invertebrate dominance in the rocky subtidal Gulf of Maine. Ecology 89:452–462

    Article  PubMed  Google Scholar 

  • Miller RJ, Etter RJ (2011) Rock walls: small-scale diversity hotspots in the subtidal Gulf of Maine. Mar Ecol Prog Ser 425:153–165

    Article  Google Scholar 

  • Miller MW, Hay ME (1996) Coral–seaweed–grazer–nutrient interactions on temperate reefs. Ecol Monogr 66:323–344

    Article  Google Scholar 

  • Miller RJ, Page HM (2012) Kelp as a trophic resource for marine suspension feeders: a review of isotope-based evidence. Mar Biol 159:1391–1402

    Article  Google Scholar 

  • Miller RJ, Reed DC, Brzezinski MA (2011) Partitioning of primary production among giant kelp (Macrocystis pyrifera), understory macroalgae, and phytoplankton on a temperate reef. Limnol Oceanogr 56:119–132

    Article  Google Scholar 

  • Miller RJ, Page HM, Brzezinski MA (2013) δ13C and δ15N of particulate organic matter in the Santa Barbara Channel: drivers and implications for trophic inference. Mar Ecol Prog Ser 474:53–66

    Article  CAS  Google Scholar 

  • Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models, 4th edn. McGraw-Hill, New York

    Google Scholar 

  • Newell R, Field J, Griffiths C (1982) Energy balance and significance of microorganisms in a kelp bed community. Mar Ecol Prog Ser 8:103–113

    Article  Google Scholar 

  • Nowell ARM, Jumars PA (1984) Flow environments of aquatic benthos. Annu Rev Ecol Syst 15:303–328

    Article  Google Scholar 

  • Orr M, Zimmer M, Jelinski DE, Mews M (2005) Wrack deposition on different beach types: spatial and temporal variation in the pattern of subsidy. Ecology 86:1496–1507

    Article  Google Scholar 

  • Page HM, Reed DC, Brzezinski MA, Melack JM, Dugan JE (2008) Assessing the importance of land and marine sources of organic matter to kelp forest food webs. Mar Ecol Prog Ser 360:47–62

    Article  Google Scholar 

  • Parnell PE, Miller EF, Lennert-Cody CE, Dayton PK, Carter ML, Stebbins TD (2010) The response of giant kelp (Macrocystis pyrifera) in southern California to low-frequency climate forcing. Limnol Oceanogr 55:2686–2702

    CAS  Google Scholar 

  • Pérez-Matus A, Ferry-Graham LA, Cea A, Vásquez JA (2008) Community structure of temperate reef fishes in kelp-dominated subtidal habitats of northern Chile. Mar Freshwater Res 58:069–1085

    Google Scholar 

  • Rau G, Riebesell U, Wolf-Gladrow D (1996) A model of photosynthetic 13C fractionation by marine phytoplankton based on diffusive molecular CO2 uptake. Mar Ecol Prog Ser 133:275–285

    Article  CAS  Google Scholar 

  • Reed DC, Foster MS (1984) The effects of canopy shading on algal recruitment and growth in a giant kelp forest. Ecology 65:937–948

    Article  Google Scholar 

  • Reed DC, Rassweiler A, Arkema KK (2008) Biomass rather than growth determines net primary production by giant kelp. Ecology 89:2493–2505

    Article  PubMed  Google Scholar 

  • Reed DC, Rassweiler A, Arkema KK (2009) Density derived estimates of standing crop and net primary production in the giant kelp Macrocystis pyrifera. Mar Biol 156:2077–2083

    Article  PubMed Central  PubMed  Google Scholar 

  • Reed DC, Rassweiler A, Carr MH, Cavanaugh KC, Malone DP, Siegel DA (2011) Wave disturbance overwhelms top-down and bottom-up control of primary production in California kelp forests. Ecology 92:2108–2116

    Article  PubMed  Google Scholar 

  • River GF, Edmunds PJ (2001) Mechanisms of interaction between macroalgae and scleractinians on a coral reef in Jamaica. J Exp Mar Biol Ecol 261:159–172

    Article  PubMed  Google Scholar 

  • Robbins IJ (1983) The effects of body size, temperature, and suspension density on the filtration and ingestion of inorganic particulate suspensions by ascidians. J Exp Mar Biol Ecol 70:65–78

    Article  Google Scholar 

  • Rosman JH, Koseff JR, Monismith SG, Grover J (2007) A field investigation into the effects of a kelp forest (Macrocystis pyrifera) on coastal hydrodynamics and transport. J Geophys Res-Oceans 112(C2):C02016

    Google Scholar 

  • Santelices B, Ojeda FP (1984) Effects of canopy removal on the understory algal community structure of coastal forests of Macrocystis pyrifera from southern South America. Mar Ecol Prog Ser 14:165–173

    Article  Google Scholar 

  • Savoye N, Aminot A, Treguer P, Fontugne M, Naulet N, Kerouel R (2003) Dynamics of particulate organic matter delta N-15 and delta C-13 during spring phytoplankton blooms in a macrotidal ecosystem (Bay of Seine, France). Mar Ecol Prog Ser 255:27–41

    Article  CAS  Google Scholar 

  • Schiel DR, Foster MS (2015) The biology and ecology of giant kelp forests. University of California Press, Berkeley

    Google Scholar 

  • Sebens KP (1986) Spatial relationships among encrusting marine organisms in the New England subtidal zone. Ecol Monogr 56:73–96

    Article  Google Scholar 

  • Seiderer LJ, Newell RC (1988) Exploitation of phytoplankton as a food resource by the kelp bed ascidian Pyura stolonifera. Mar Ecol Prog Ser 50:107–115

    Article  Google Scholar 

  • Shears NT, Babcock RC (2002) Marine reserves demonstrate top-down control of community structure on temperate reefs. Oecologia 132:131–142

    Article  Google Scholar 

  • Shepherd S, Edgar G (2013) Ecology of Australian temperate reefs: the unique south. CSIRO, Collingwood

    Google Scholar 

  • 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 29:436–459

    Article  Google Scholar 

  • Tallis H (2009) Kelp and rivers subsidize rocky intertidal communities in the Pacific Northwest (USA). Mar Ecol Prog Ser 389:85–96

    Article  Google Scholar 

  • Tanner JE (1995) Competition between scleractinian corals and macroalgae: an experimental investigation of coral growth, survival and reproduction. J Exp Mar Biol Ecol 190:151–168

    Article  Google Scholar 

  • Velimirov B, Field JG, Griffiths CL, Zoutendyk P (1977) The ecology of kelp bed communities in the Benguela upwelling system. Helgol Meer 30:495–518

    Article  Google Scholar 

  • Vetter EW, Dayton PK (1998) Macrofaunal communities within and adjacent to a detritus-rich submarine canyon system. Deep-Sea Res Part II 45:25–54

    Article  Google Scholar 

  • Wallace JB, Webster JR, Eggert SL et al (2001) Large woody debris in a headwater stream: long-term legacies of forest disturbance. Int Rev Hydrobiol 86:501–513

    Article  Google Scholar 

  • Wernberg T, Kendrick GA, Toohey BD (2005) Modification of the physical environment by an Ecklonia radiata (Laminariales) canopy and implications for associated foliose algae. Aquat Ecol 39:419–430

    Article  Google Scholar 

  • Yorke CE, Miller RJ, Page HM, Reed DC (2013) Importance of kelp detritus as a component of suspended particulate organic matter in giant kelp Macrocystis pyrifera forests. Mar Ecol Prog Ser 493:113–125

    Article  CAS  Google Scholar 

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Acknowledgments

We thank S. Harrer, P. Laverty, C. Nelson, C. Santschi, N. Schooler, A. Wang, and K. Yager for field and laboratory assistance. The University of California Santa Barbara Marine Science Institute Analytical Laboratory analyzed samples for stable isotopes. This work was supported by the US National Science Foundation’s Long-Term Ecological Research Program and by NSF OCE 0962306 to H. M. P. and R. J. M.

Author contribution statement

R. J. M., H. M. P. and D. C. R. conceived and designed the experiments. R. J. M. and H. M. P. performed the experiments. R. J. M. analyzed the data. R. J. M., H. M. P. and D. C. R. wrote the manuscript.

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  1. Marine Science Institute, University of California, Santa Barbara, CA, USA

    Robert J. Miller, Henry M. Page & Daniel C. Reed

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  1. Robert J. Miller
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  2. Henry M. Page
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Correspondence to Robert J. Miller.

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Communicated by Helene Marsh.

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Miller, R.J., Page, H.M. & Reed, D.C. Trophic versus structural effects of a marine foundation species, giant kelp (Macrocystis pyrifera). Oecologia 179, 1199–1209 (2015). https://doi.org/10.1007/s00442-015-3441-0

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