Skip to main content
Log in

Relative effects of nutrient enrichment and grazing on epiphyte-macrophyte (Zostera marina L.) dynamics

  • Original Papers
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The independent and interactive effects of nutrient concentration and epiphyte grazers on epiphyte biomass and macrophyte growth and production were examined in Zostera marina L. (eelgrass) microcosms. Experiments were conducted during early summer, late summer, fall, and spring in a greenhouse on the York River estuary of Chesapeake Bay. Nutrient treatments consisted of ambient or enriched (3× ambient) concentrations of inorganic nitrogen (ammonium nitrate) and phosphate. Grazer treatments consisted of the presence or absence of field densities of isopods, amphipods, and gastropods. epiphyte biomass increased with both grazer removal and nutrient enrichment during summer and spring experiments. The effect of grazers was stronger than that of nutrients. There was little epiphyte response to treatment during the fall, a result possibly of high ambient nutrient concentrations and low grazing pressure. Under low grazer densities of early summer, macrophyte production (g m−2 d−1) was reduced by grazer removal and nutrient enrichment independently. Under high grazer densities of late summer, macrophyte production was reduced by enrichment only with grazers absent. During spring and fall there were no macrophyte responses to treatment. The relative influence of epiphytes on macrophyte production may have been related to seasonally changing water temperature and macrophyte requirements for light and inorganic carbon.

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.

Similar content being viewed by others

References

  • Barko JW, Adams MS, Clesceri NL (1986) Environmental factors and their consideration in the management of submersed aquatic vegetation: a review. J Aquat Plant Manage 24:1–10

    Google Scholar 

  • Batuik R, Heasly P, orth R, Moore K, Capelli J, Stevenson C, Dennison W, Staver L, Carter V, Rybicki N, Hickman R, Kollar S, Bieber S (1993) Chesapeake Bay submerged aquatic vegetation habitat requirements and restoration targets: a technical synthesis. U S Environ Prot Agency Chesapeake Bay Program, Annapolis, MD. CPB Tech Rep Ser (in press)

  • Borum J (1987) Dynamics of epiphyton on eelgrass (Zostera marina L.) leaves: relative roles of algal growth, herbivory, and substratum turnover. Limnol Oceanogr 32:986–992

    Google Scholar 

  • Borum J, Wium-Andersen S (1980) Biomass and production of epiphytes on eelgrass (Zostera marina L.) in the Oresund, Denmark. Ophelia Suppl 1:57–64

    Google Scholar 

  • Borum J, Kaas H, Wium-Andersen S (1984) Biomass variation and autotrophic production of an epiphyte-macrophyte community in a coastal Danish area: II. Epiphyte species composition, biomass and production. Ophelia 23:165–179

    Google Scholar 

  • Brönmark C (1985) Interactions between macrophytes, epiphytes and herbivores: an experimental approach. Oikos 45:26–30

    Google Scholar 

  • Bulthuis DA, Woelkerling WJ (1983) Biomass accumulation and shading effects of epiphytes on leaves of the seagrass, Heterozostera tasmanica, in Victoria, Australia. Aquat Bot 16:137–148

    Google Scholar 

  • Cambridge ML, Chiffings AW, Brittan C, Moore L, McComb AJ (1986) The loss of seagrass in Cockburn Sound, Western Australia. II. Possible causes of seagrass decline. Aquat Bot 24:269–285

    Google Scholar 

  • Carpenter SR (1980) The decline of Myriophyllum spicatum in a eutrophic Wisconsin lake. Can J Bot 58:527–535

    Google Scholar 

  • Carpenter SR (1988) Complex interactions in lake communities. Springer, New York

    Google Scholar 

  • Carrick HJ, Lowe RL (1989) Benthic algal response to N and P enrichment along a pH gradient. Hydrobiologia 179:119–127

    Google Scholar 

  • Cattaneo A (1983) Grazing on epiphytes. Limnol Oceanogr 28:124–132

    Google Scholar 

  • Cattaneo A (1987) Periphyton in lakes of different trophy. Can J Fish Aquat Sci 44:296–303

    Google Scholar 

  • Cattaneo A, Kalff J (1986) The effect of grazer size manipulation on periphyton communities. Oecologia 69:612–617

    Google Scholar 

  • Colletti PJ, Blinn DW, Pickart A, Wagner VT (1987) Influence of different densities of the mayfly grazer Heptagenia criddlei on lotic diatom communities. J N Am Benthol Soc 6:270–280

    Google Scholar 

  • Cuker BE (1983) Grazing and nutrient interactions in controlling the activity and composition of the epilithic algal community of an arctic lake. Limnol Oceanogr 28:133–141

    Google Scholar 

  • DeNicola DM, McIntire CD, Lamberti GA, Gregory SV, Ashkenas LR (1990) Temporal patterns of grazer-periphyton interactions in laboratory streams. Freshwater Biol 23:475–489

    Google Scholar 

  • Dennison WC, Alberte RS (1982) Photosynthetic responses of Zostera marina L. (eelgrass) to in situ manipulations of light intensity. Oecologia 55:137–144

    Google Scholar 

  • Duffy JE (1990) Amphipods on seaweeds: partners or pests? Ocologia 83:267–276

    Google Scholar 

  • Eminson D, Phillips G (1978) A laboratory experiment to examine the effects of nutrient enrichment on macrophyte and epiphyte growth. Verh Internat Verein Limnol 20:82–87

    Google Scholar 

  • Fairchild GW, Everett AC (1988) Effects of nutrient (N, P, C) enrichment upon periphyton standing crop, species composition and primary production in an oligotrophic softwater lake. Freshwater Biol 19:57–70

    Google Scholar 

  • Fairchild GW, Lowe RL, Richardson WB (1985) Algal periphyton growth on nutrient-diffusing substrates: an in situ bioassay. Ecology 66:465–472

    Google Scholar 

  • Fonseca MS, Zieman JC, Thayer GW, Fisher JS (1983) The role of current velocity in structuring eelgrass (Zostera marina L.) meadows. Estuarine Coastal Shelf Sci 17:367–380

    Google Scholar 

  • Giesy JP Jr, Odum EP (1980) Microcosmology: introductory comments. In: Giesy JP Jr (ed) Microcosms in ecological research. Technical Information Center, U.S. Dep. of Energy, Symposium Series No. 52, pp 1–13

  • Harlin MM, Thorne-Miller B (1981) Nutrient enrichment of seagrass beds in a Rhode Island coastal lagoon. Mar Biol 65:221–229

    Google Scholar 

  • Hart DD, Robinson CT (1990) Resource limitation in a stream community: phosphorus enrichment effects on periphyton and grazers. Ecology 71:1494–1502

    Google Scholar 

  • Heijs FML (1984) Annual biomass and production of epiphytes in three monospecific seagrass communities of Thalassia hemprichii (Ehrenb.) Aschers. Aquat Bot 20:195–218

    Google Scholar 

  • Hill WR, Knight AW (1988) Concurrent grazing effects of two stream insects on periphyton. Limnol Oceanogr 33:15–26

    Google Scholar 

  • Hillman K, Walker DI, Larkum AWD, McComb AJ (1989) Productivity and nutrient limitation. In: Larkum AWD, McComb AJ, Sheperd SA (eds) Biology of Seagrasses. Elsevier Science Publishers B V, Amsterdam, pp 635–685

    Google Scholar 

  • Hootsmans MJM, Vermaat JE (1985) The effect of periphytongrazing by three epifaunal species on the growth of Zostera marina L. under experimental conditions. Aquat Bot 22:83–88

    Google Scholar 

  • Hough RA, Fornwall MD, Negele BJ, Thompson RL, Putt DA (1989) Plant community dynamics in a chain of lakes: principal factors in the decline of rooted macrophytes with eutrophication. Hydrobiologia 173:199–217

    Google Scholar 

  • Howard RK (1982) Impact of feeding activities of epibenthic amphipods on surface-fouling of eelgrass leaves. Aquat Bot 14:91–97

    Google Scholar 

  • Howard RK, Short FT (1986) Seagrass growth and survivorship under the influence of epiphyte grazers. Aquat Bot 24:287–302

    Google Scholar 

  • Jacoby JM (1987) Alterations in periphyton characteristics due to grazing in a Cascade foothill stream. Freshwater Biol 18:495–508

    Google Scholar 

  • Kairesalo T, Koskimies I (1987) Grazing by oligochaetes and snails on epiphytes. Freshwater Biol 17:317–324

    Google Scholar 

  • Kemp WM, Boynton WR, Twilley RR, Stevenson JC, Means JC (1983) The decline of submerged vascular plants in upper Chesapeake Bay: summary of results concerning possible causes. Mar Technol Soc J 17:78–89

    Google Scholar 

  • Kentula ME, McIntire CD (1986) The autecology and production dynamics of eelgrass (Zostera marina L.) in Netarts Bay, Oregon. Estuaries 9:188–199

    Google Scholar 

  • Kerfoot WC, Sih A (1987) Predation: direct and indirect impacts on aquatic communities. University Press of New England, Hanover

    Google Scholar 

  • Lamberti GA, Resh VH (1983) Stream periphyton and insect herbivores: an experimental study of grazing by a caddisfly population. Ecology 64:1124–1135

    Google Scholar 

  • Lamberti GA, Ashkenas LR, Gregory SV, Steinman AD (1987) Effects of three herbivores on periphyton communities in laboratory streams. J N Am Benthol Soc 6:92–104

    Google Scholar 

  • Lodge DM, Barko JW, Strayer D, Melack JM, Mittelbach GG, Howarth RW, Menge B, Titus JE (1988) Spatial heterogeneity and habitat interactions in lake communities. In: Carpenter SR (ed) Complex interactions in lake communities. Springer, New York, pp 181–208

    Google Scholar 

  • Losee RF, Wetzel RG (1983) Selective light attenuation by the periphyton complex. In: Wetzel RG (ed) Periphyton of freshwater ecosystems. Dr W Junk Publishers, The Hague, pp 89–96

    Google Scholar 

  • Lowe RL, Hunter RD (1988) Effect of grazing by Physa integra on periphyton community structure. J N Am Benthol Soc 7:29–36

    Google Scholar 

  • Marks JC, Lowe RL (1989) The independent and interactive effects of snail grazing and nutrient enrichment on structuring periphyton communities. Hydrobiologia 185:9–17

    Google Scholar 

  • Marsh GA (1973) The Zostera epifaunal community in the York River, Virginia. Ches Sci 14:87–97

    Google Scholar 

  • Marsh JA Jr, Dennison WC, Alberte RS (1986) Effects of temperature on photosynthesis and respiration in eelgrass (Zostera marina L.) J Exp Mar Biol Ecol 101:257–267

    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 

  • Mazumder A, Taylor WD, McQueen DJ, Lean DRS (1989) Effects of nutrients and grazers on periphyton phosphorus in lake enclosures. Freshwater Biol 22:405–415

    Google Scholar 

  • Montfrans J van, Orth RJ, Vay SA (1982) Preliminary studies of grazing by Bittium varium on eelgrass periphyton. Aquat Bot 14:75–89

    Google Scholar 

  • Mulholland PJ, Steinman AD, Palumbo AV, Elwood JW (1991) Role of nutrient cycling and herbivory in regulating periphyton communities in laboratory streams. Ecology 72:966–982

    Google Scholar 

  • Murray L, Wetzel RL (1987) Oxygen production and consumption associated with the major autotrophic components in two temperate seagrass communities. Mar Ecol Prog Ser 38:231–239

    Google Scholar 

  • Neckles HA (1990) Relative effects of nutrient enrichment and grazing on epiphyton-macrophyte (Zostera marina L.) dynamics. PhD dissertation, College of William and Mary, Williamsburg, Virginia

  • Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models. Richard D Irwin, Inc, Homewood, Illinois

    Google Scholar 

  • Nicotri ME (1977) Grazing effects of four marine intertidal herbivores on the microflora. Ecology 58:1020–1032

    Google Scholar 

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

    Google Scholar 

  • Orth RJ, Moore KA (1986) Seasonal and year-to-year variations in the growth of Zostera marina L. (eelgrass) in the lower Chesapeake Bay. Aquat Bot 24:335–341

    Google Scholar 

  • Orth RJ, van Montfrans J (1984) Epiphyte-seagrass relationships with an emphasis on the role of micrograzing: a review. Aquat Bot 18:43–69

    Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford

    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 

  • Phillips GL, Eminson D, Moss B (1978) A mechanism to account for macrophyte decline in progressively eutrophicated freshwaters. Aquat Bot 4:103–126

    Google Scholar 

  • Potvin C, Lechowicz MJ, Tardif S (1990) The statistical analysis of ecophysiological response curves obtained from experiments involving repeated measures. Ecology 71:1389–1400

    Google Scholar 

  • Pringle CM (1987) Effects of water and substratum nutrient supplies on lotic periphyton growth: an integrated bioassay. Can J Fish Aquat Sci 44:619–629

    Google Scholar 

  • Power ME (1990) Resource enhancement by indirect effects of grazers: armored catfish, algae, and sediment. Ecology 71:897–904

    Google Scholar 

  • Rogers KH, Breen CM (1983) An investigation of macrophyte, epiphyte and grazer interactions. In: Wetzel RG (ed) Periphyton of freshwater ecosystems. Dr W Junk Publishers, The Hague, pp 217–226

    Google Scholar 

  • Sand-Jensen K (1975) Biomass, net production and growth dynamics in an eelgrass (Zostera marina L.) population in Vellerup Vig, Denmark. Ophelia 14:185–201

    Google Scholar 

  • Sand-Jensen K (1977) Effect of epiphytes on eelgrass photosynthesis. Aquat Bot 3:55–63

    Google Scholar 

  • Sand-Jensen K (1983) Physical and chemical parameters regulating growth of periphytic communities. In: Wetzel RG (ed) Periphyton of freshwater ecosystems. Dr W Junk Publishers, The Hague, pp 63–71

    Google Scholar 

  • Sand-Jensen K, Borum J (1984) Epiphyte shading and its effect on photosynthesis and diel metabolism of Lobelia dortmanna L. during the spring bloom in a Danish Lake. Aquat Bot 20:109–119

    Google Scholar 

  • Sand-Jensen K, Borum J (1991) Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries. Aquat Bot 41:137–175

    Google Scholar 

  • Sand-Jensen K, Revsbech NP (1987) Photosynthesis and light adaptation in epiphyte-macrophyte associations measured by oxygen microelectrodes. Limnol Oceanogr 32:452–457

    Google Scholar 

  • Sand-Jensen K, Søndergaard M (1981) Phytoplankton and epiphyte development and their shading effect on submerged macrophytes in lakes of different nutrient status. Int Rev Ges Hydrobiol 66:529–552

    Google Scholar 

  • SAS (1987) SAS/STAT guide for personal computers, version 6 edition. SAS Institute Inc, Cary, North Carolina

    Google Scholar 

  • Shoaf WT, Lium BW (1976) Improved extraction of chlorophyll a and b from algae using dimethyl sulfoxide. Limnol Oceanogr. 21:926–928

    Google Scholar 

  • Silberstein K, Chiffings AW, McComb AJ (1986) The loss of seagrass in Cockburn Sound, Western Australia. III. The effect of epiphytes on productivity of Posidonia australis Hook. f. Aquat Bot 24:355–371

    Google Scholar 

  • Steinman AD, McIntire CD, Gregory SV, Lamberti GA, Ashkenas LR (1987) Effects of herbivore type and density on taxonomic structure and physiognomy of algal assemblages in laboratory streams. J N Am Benthol Soc 6:175–188

    Google Scholar 

  • Stewart AJ (1987) Responses of stream algae to grazing minnows and nutrients: a field test for interactions. Oecologia 72:1–7

    Google Scholar 

  • Sumner ET, McIntire CD (1982) Grazer-periphyton interactions in laboratory streams. Arch Hydrobiol 93:135–157

    Google Scholar 

  • Thayer GW, Kenworthy WJ, Fonseca MS (1984) The ecology of eelgrass meadows of the Atlantic coast: a community profile. U S Fish Wildl Serv FWS/OBS-84/02

  • Tomasko DA, Lapointe BE (1991) Productivity and biomass of Thalassia testudinum as related to water column nutrient availability: field observations and experimental studies. Mar Ecol Prog Ser 75:9–17

    Google Scholar 

  • Twilley RR, Kemp WM, Staver KW, Stevenson JC, Boynton WR (1985) Nutrient enrichment of estuarine submersed vascular plant communities. 1. Algal growth and effects on production of plants and associated communities. Mar Ecol Prog Ser 23:179–191

    Google Scholar 

  • USEPA (1979) Methods for chemical analysis of water and wastes. U S Environ Prot Agency EPA-600/4-79-020

  • Wetzel RL, Neckles HA (1986) A model of Zostera marina L. photosynthesis and growth: simulated effects of selected physical-chemical variables and biological interactions. Aquat Bot 26:307–323

    Google Scholar 

  • Wetzel RL, Penhale PA (1983) Production ecology of seagrass communities in the lower Chesapeake Bay. Mar Tech Soc J 17:22–31

    Google Scholar 

  • Winer BJ (1971) Statistical principles in experimental design. McGraw-Hill, Inc, New York

    Google Scholar 

  • 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 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Neckles, H.A., Wetzel, R.L. & Orth, R.J. Relative effects of nutrient enrichment and grazing on epiphyte-macrophyte (Zostera marina L.) dynamics. Oecologia 93, 285–295 (1993). https://doi.org/10.1007/BF00317683

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00317683

Key words

Navigation