Skip to main content
SpringerLink
Log in

Top-down impact through a bottom-up mechanism: the effect of limpet grazing on growth, productivity and carbon allocation of Zostera marina L. (eelgrass)

  • Plant Animal Interactions
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The unusual appearance of a commensal eelgrass limpet [Tectura depicta (Berry)] from southern California at high density (up to 10 shoot−1) has coincided with the catastrophic decline of a subtidal Zostera marina L. meadow in Monterey Bay, California. Some commensal limpets graze the chloroplast-rich epidermis of eelgrass leaves, but were not known to affect seagrass growth or productivity. We evaluated the effect on eelgrass productivity of grazing by limpets maintained at natural densities (8±2 shoot−1) in a natural light mesocosm for 45 days. Growth rates, carbon reserves, root proliferation and net photosynthesis of grazed plants were 50–80% below those of ungrazed plants, but biomass-specific respiration was unaffected. The daily period of irradiance-saturated photosynthesis (H sat) needed to maintain positive carbon balance in grazed plants approached 13.5 h, compared with 5–6 h for ungrazed plants. The amount of carbon allocated to roots of ungrazed plants was 800% higher than for grazed plants. By grazing the chlorophyll-rich epidermis, T. depicta induced carbon limitation in eelgrass growing in an other-wise light-replete environment. Continued northward movement of T. depicta, may have significant impacts on eelgrass production and population dynamics in the northeast Pacific, even thought this limpet consumes very little plant biomass. This interaction is a dramatic example of top-down control (grazing/predation) of eelgrass productivity and survival operating via a bottom-up mechanism (photosynthesis limitation).

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Backman TW, Barilotti DC (1976) Irradiance reduction: effects on standing crops of the eelgrass Zostera marina in a coastal lagoon. Mar Biol 34:33–40

    Google Scholar 

  • Barbour MG, Radosevich SR (1979) 14C uptake by the marine angiosperm Phyllospadix scouleri. Am J Bot 66:301–306

    Google Scholar 

  • Barry JP, Baxter CH, Sagarin RD, Gilman SE (1995) Long-term faunal changes in a California rocky intertidal community. Science 267:672–675

    Google Scholar 

  • Batiuk RA, Orth RJ, Moore KA, Dennison WC, Stevenson JC, Staver LM, Carter V, et al. (1993) Chesapeake Bay submerged aquatic vegetation habitat requirements and restoration targets: a technical synthesis (Chesapeake Bay Program). US Environment Protection Agency, Annapolis

    Google Scholar 

  • Branch GM, Branch MI (1980) Competition between Cellana tramoserica (Sowerby) (Gastropoda) and Patiriella exigua (Lamarck) (Asteroidea) and their influence on algal standing stocks. J Exp Mar Biol Ecol 48:35–49

    Google Scholar 

  • Busby D, Virnstein RW (1993) SAVI excecutive summary. In: Morris LJ, Tomasko DA (eds) Proceedings and conclusions of workshops on: submerged aquatic vegetation initiative and photosynthetically active radiation. St Johns River Water Management District, Palatka, Florida, pp iii-viii

    Google Scholar 

  • Carlton JT, Vermeij GT, Lindberg DR, Carlton DA, Dudley EC (1991) The first historical extinction of a marine invertebrate in an ocean basin: the demise of the eelgrass limpet Lottia alveus. Biol Bull 180:72–80

    Google Scholar 

  • Chu CC, Coleman JS, Mooney HA (1992) Controls of biomass partitioning between roots and shoots: atmospheric carbon dioxide enrichment and the acquisition and allocation of carbon in the wild radish. Oecologia 89:580–587

    Google Scholar 

  • Dayton PK (1971) Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol Monogr 41:351–389

    Google Scholar 

  • Dennison WC, Alberte RS (1985) Role of daily light period in the depth distribution of Zostera marina L. (eelgrass). Mar Ecol Prog Ser 25:51–61

    Google Scholar 

  • Dennison WC, Alberte RS (1986) Photoadaptation and growth of Zostera marina L. (eelgrass) transplants along a depth gradient. J Exp Mar Biol Ecol 98:265–282

    Google Scholar 

  • Dennison WC, Orth RJ, Moore KA, Stevenson JC, Carter V, Kollar S, Bergstrom PW, Batiuk RA (1993) Assessing water quality with submersed aquatic vegetation. Habitat requirements as barometers of Chesapeake Bay health. BioScience 43:86–94

    Google Scholar 

  • Duarte CM (1991) Seagrass depth limits. Aquat Bot 40:363–377

    Google Scholar 

  • Dunton KH (1995) Seasonal growth and biomas of the subtropical seagrass Halodule wrightii in relation to continuous measurements of underwater irradiance. Mar Biol 120:479–489

    Google Scholar 

  • Fishlyn D, Phillips DW (1980) Chemical camouflaging and behavioral defenses against a predatory seastar by three species of gastropods from the surfgrass Phyllospsadix community. Biol Bull 158:34–48

    Google Scholar 

  • Gleeson SK, Tilman D (1992) Plant allocation and the multiple limitation hypothesis. Am Nat 139:1322–1343

    Google Scholar 

  • Hartog C den (1994) Suffocation of a littoral Zostera bed by Enteromorpha radiata. Aquat Bot 47:21–28

    Google Scholar 

  • Heilmeier H, Freund M, Steinlein T, Schulze ED, Monson RK (1994) The influence of nitrogen availability on carbon and nitrogen storage in the biennial Cirsium vulgare (Savi) Ten. I. Storage capacity in relation to resource acquisition, allocation and recycling. Plant Cell Environ 17:1125–1131

    Google Scholar 

  • Huber SC (1989) Biochemical mechanism for regulation of sucrose accumulation in leaves during photosynthesis. Plant Physiol 91:656–662

    Google Scholar 

  • Huber SC, Huber JL (1992) Role of sucrose-phosphate synthetase in sucrose metabolism in leaves. Plant Physiol 99:1275–1279

    Google Scholar 

  • Huber SC, Israel DW (1982) Biochemical basis for partitioning of photosynthetically fixed carbon between starch and sucrose in soybean (Glycine max Meer.) leaves. Plant Physiol 69:691–696

    Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for the determination of chlorophylls a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    Google Scholar 

  • Kenworthy WJ, Haunert DE (1991) The light requirements of seagrasses: proceedings of a workshop to examine the capabality of water quality criteria, standards and monitoring programs to protect seagrasses (Technical Memorandum NMFS-SEFC-287). “National Oceanic and Atmospheric Administration”, Beaufort, North Carolina

    Google Scholar 

  • Klumpp DW, Salita-Espinosa JT, Fortes MD (1993) Feeding ecology and trophic role of sea urchins in a tropical seagrass community. Aquat Bot 45:205–229

    Google Scholar 

  • Kraemer GP, Alberte RS (1993) Age-related patterns of metabolism and biomass in subterranean tissues of Zostera marina L. (eelgrass). Mar Ecol Prog Ser 95:193–203

    Google Scholar 

  • Lindberg DR (1980) Notoacmea gabitella (Berry), an outer coast form of Notoacmea depicta (Hinds) (Mollusca: Acmaeidae). Veliger 22:265–272

    Google Scholar 

  • Mann KH (1982) Ecology of coastal waters. A systems approach. University of California Press, Berkeley

    Google Scholar 

  • Mazzella L, Alberte RS (1986) Light adaptation and the role of autotrophic epiphytes in primary production of the temperate seagrass, Zostera marina L. J Exp Mar Biol Ecol 100:165–180

    Google Scholar 

  • Mazzella L, Buia MC (1980) Variazoni a lungo termine in alcuni parametric strutturali di una prateria a Posidonia oceanica. Nova Thalassia 10 (Suppl 1):533–542

    Google Scholar 

  • Mazzella L, Mauzerall D, Lyman H, Alberte RS (1981) Protoplast isolation and photosynthetic characteristics of Zostera marina L. (eelgrass). Bot Mar 23:285–289

    Google Scholar 

  • McRoy CP (1969) Eelgrass under Arctic winter ice. Nature 224:818–819

    Google Scholar 

  • Menge BA (1976) Organization of the New England rocky intertidal community: role of predation, competition and environmental heterogencity. Ecol Monogr 42:355–393

    Google Scholar 

  • Menge BA (1992) Community regulation: under what conditions are botton-up factors important on rocky shores? Ecology 73:755–765

    Google Scholar 

  • Morris LJ, Tomasko DA (1993) Proceedings and conclusions of workshops on: submerged aquatic vegetation initiative and photosynthetically active radiation (Special Publication SJ93-SP13). St Johns River Water Management District, Palatka, Florida

    Google Scholar 

  • Neckles HA, Wetzel RL, Orth RJ (1993) Relative effects of nutrient enrichment and grazing on epiphyte-macrophyte (Zostera marina L.) dynamics. Oecologia 36:265–274

    Google Scholar 

  • Orth RJ, Moore KA (1983) Chesapeake Bay: an unprecedenced decline in submerged aquatic vegetation. Science 222:51–53

    Google Scholar 

  • Penhale PA (1977) Macrophyte-epiphyte biomass and productivity in an eelgrass (Zostera marina L.) community. J Exp Mar Biol Ecol 26:211–224

    Google Scholar 

  • Pergent G, Boudouresque CF, Thelin I, Marchadour M, Pergent-Martini C (1991) Map of benthic vegetation and seabottom types in the bay at Banyuls-Sur-Mer. Vie Milieu 41:165–186

    Google Scholar 

  • Provancha JA, Hall CR (1991) Observations of associations between seagrass beds and manatees in east central Florida. Fla Sci 54:87–98

    Google Scholar 

  • Rasmussen E (1977) The wasting disease of eelgrass (Zostera marina) and its effect on environmental factors and fauna. In: McRoy CP, Helffrich C (eds) Seagrass ecosystems, a scientific perspective. Marcel Dekker, New York, pp 1–51

    Google Scholar 

  • Reekie EG, Bazzaz FA (1989) Competition and patterns of resource use among seedlings of five tropical trees grown at ambient and elevated carbon dioxide. Oecologia 79:212–222

    Google Scholar 

  • Roemmich D, McGowan JA (1995) Climatic warming and the decline of zoolankton in the California Current. Science 267:1324–1326

    Google Scholar 

  • Shepherd SA, McComb AJ, Bulthuis DA, Neverauskus V, Steffensen DA, West R (1989) Decline of seagrasses. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of seagrasses. A treatise on the biology of seagrasses with special reference to the Australian region. Elsevier, Amsterdam, pp 346–393

    Google Scholar 

  • Smith RD, Pregnall AM, Alberte RS (1988) Effects of anaerobiosis on root metabolism of the seagrass Zostera marina L. (eelgrass). Mar Biol 98:131–141

    Google Scholar 

  • Tomlinson PB (1980) Leaf morphology in seagrasses. In: Phillips RC, McRoy CP (eds) Handbook of seagrass biology. An ecosystem perspective. Garland, New York, pp 7–28

    Google Scholar 

  • Tunberg BG, Nelson WG, Smith G (1994) Population ecology of Pagurus maclaughlinae Garcia-Gomez (Decapoda: Anomura: Paguridae) in the Indian River Laggon, Florida. J Crustacean Biol 14:686–699

    Google Scholar 

  • Underwood AJ (1980) The effect of grazing by gastropods and physical factors on the upper limit of distribution of intertidal macroalgae. Oecologia 46:201–213

    Google Scholar 

  • Underwood AJ, Denley EJ, Moran AJ (1983) Experimental analyses of the structure and dynamics of mid-shore rocky intertidal communities in New South Wales. Oecologia 56:202–219

    Google Scholar 

  • Williams SL (1988) Thalassia testudinum productivity and grazing by green turtles in a highly disturbed seagrass bed. Mar Biol 98:447–456

    Google Scholar 

  • Winterbourne DJ (1986) Cell growth determined by a dye-binding assay. Biochem Soc Trans 14:1179

    Google Scholar 

  • Wolters V, Stickan W (1991) Resource allocation of beech seedlings (Fagus sylvatica L.): relationship to earthworm activity and soil conditions. Oecologia 88:125–131

    Google Scholar 

  • zimmerman RC, Alberte RS (in 1996) Effect of light/dark transition on carbon translocation in eelgrass (Zostera marina L.) seedlings. Mar Ecol Prog Ser (in press)

  • Zimmerman RC, Smith RD, Alberte RS (1989) Thermal acclimation and whole plant carbon balance in Zostera marina L. (eelgrass). J Exp Mar Biol Ecol 130:93–109

    Google Scholar 

  • Zimmerman RC, Reguzzoni JL, Wyllie-Echeverria S, Josselyn M, Alberte RS (1991) Assessment of environmental suitability for growth of Zostera marina L. (eeglgrass) in San Francisco Bay. Aquat Bot 39:353–366

    Google Scholar 

  • Zimmerman RC, Cabello-Pasini A, Alberte RS (1994) Modeling daily production of aquatic macrophytes from irradiance measurements: a comparative analysis. Mar Ecol Prog Ser 114:185–196

    Google Scholar 

  • Zimmerman RC, Kohrs DG, Steller DL, Alberte RS (1995a) Carbon partitioning in the seagrass Zostera marina: Regulation by photosynthesis and the response to daily ligh-dark cycles. Plant Physiol 108:1665–1671

    Google Scholar 

  • Zimmerman RC, Reguzzoni JL, Alberte RS (1995b) Eelgrass (Zostera marina L.) transplants in San Francisco Bay: role of light availability on metabolism, growth and survival. Aquat Bot 51:67–86

    Google Scholar 

Download references

Author information

Author notes

  1. Richard C. Zimmerman

    Present address: Hopkins Marine Station, 93950, Pacific Grove, CA, USA

  2. Randall S. Alberte

    Present address: Biological Science and Technology Program, Office of Naval Research, 22217, Arlington, VA, USA

Authors and Affiliations

  1. Biology Department, University of California, 90024, Los Angeles, CA, USA

    Richard C. Zimmerman, Donald G. Kohrs & Randall S. Alberte

Authors
  1. Richard C. Zimmerman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Donald G. Kohrs
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Randall S. Alberte
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richard C. Zimmerman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zimmerman, R.C., Kohrs, D.G. & Alberte, R.S. Top-down impact through a bottom-up mechanism: the effect of limpet grazing on growth, productivity and carbon allocation of Zostera marina L. (eelgrass). Oecologia 107, 560–567 (1996). https://doi.org/10.1007/BF00333949

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00333949

Key words

Search

Navigation