Skip to main content

Advertisement

SpringerLink
Log in

Herbivore impacts on two morphologically similar bloom-forming Ulva species in a eutrophic bay

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Herbivore impacts on macrophyte growth vary with the identity of the herbivores and macrophytes, as well as under different abiotic conditions. This interaction is further complicated by anthropogenic alterations to the environment, such as eutrophication. In this study, we utilized in situ herbivore exclusion experiments and mesocosm feeding preference assays to examine the impacts of different herbivores on the growth of two morphologically similar, co-occurring macroalgal bloom Ulva species in a nutrient-rich environment. We found that herbivory had a measurable impact on Ulva biomass, though the rate of consumption rarely surpassed growth for either Ulva species. We determined that the primary herbivores within the blooms were amphipods and mud crabs, and that their effects varied among study sites and months. Our results also confirmed that, even with a diverse suite of consumers, Ulva blooms are capable of escaping herbivore control, particularly early in the growing season when growth rates peak and herbivore activity is limited. Furthermore, our experiments revealed species-specific feeding preferences among herbivores, as well as differences in growth rates and chemistry between the two Ulva species, which likely influence bloom dynamics.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aquilino, K., M. Bracken, M. Faubel & J. Stachowicz, 2009. Local-scale nutrient regeneration facilitates seaweed growth on wave-exposed rocky shores in an upwelling system. Limnology and Oceanography 54: 309–317.

    Article  Google Scholar 

  • Berezina, N. A., I. G. Tsiplenkina, E. S. Pankova & J. I. Gubelit, 2007. Dynamics of invertebrate communities on the stony littoral of the Neva Estuary (Baltic Sea) under macroalgal blooms and bioinvasions. Transitional Waters Bulletin 1: 65–76.

    Google Scholar 

  • Boyer, K., P. Fong, A. Armitage & R. Cohen, 2004. Elevated nutrient content of tropical macroalgae increases rates of herbivory in coral, seagrass, and mangrove habitats. Coral Reefs 23: 530–538.

    Google Scholar 

  • Burkepile, D. E. & M. E. Hay, 2006. Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87: 3128–3139.

    Article  PubMed  Google Scholar 

  • Burkepile, D. E. & M. E. Hay, 2010. Impact of herbivore identity on algal succession and coral growth on a Caribbean reef. PLoS One 5: e8963.

    Article  PubMed Central  PubMed  Google Scholar 

  • Calabretta, C. J. & C. A. Oviatt, 2008. The response of benthic macrofauna to anthropogenic stress in Narragansett Bay, Rhode Island: a review of human stressors and assessment of community conditions. Marine Pollution Bulletin 56: 1680–1695.

    Article  CAS  PubMed  Google Scholar 

  • Deacutis, C., 2008. Evidence of ecological impacts from excess nutrients in upper Narragansett Bay. In Desbonnet, A. & B. A. Costa-Pierce (eds), Science for Ecosystem-Based Management. Springer, New York: 349–381.

    Chapter  Google Scholar 

  • Dudley, T. L., 1992. Beneficial effects of herbivores on stream macroalgae via epiphyte removal. Oikos 65: 121–127.

    Article  Google Scholar 

  • Duffy, J. E. & M. E. Hay, 1991. Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology 72: 1286–1298.

    Article  Google Scholar 

  • Duffy, J. E. & A. M. Harvilicz, 2001. Species-specific impacts of grazing amphipods in an eelgrass-bed community. Marine Ecology Progress Series 223: 201–211.

    Article  Google Scholar 

  • Duffy, J. E., K. S. MacDonald, J. M. Rhode & J. D. Parker, 2001. Grazer diversity, functional redundancy, and productivity in seagrass beds: an experimental test. Ecology 82: 2417–2434.

    Article  Google Scholar 

  • Erickson, A. A., V. J. Paul, K. L. Van Alstyne & L. M. Kwiatkowski, 2006. Palatability of macroalgae that use different types of chemical defenses. Journal of Chemical Ecology 32: 1883–1895.

    Article  CAS  PubMed  Google Scholar 

  • Fox, S. E., M. Teichberg, I. Valiela & L. Heffner, 2012. The relative role of nutrients, grazing, and predation as controls on macroalgal growth in the Waquoit Bay estuarine system. Estuaries and Coasts 35: 1193–1204.

    Article  CAS  Google Scholar 

  • Geertz-Hansen, O., K. Sand-Jensen, D. F. Hansen & A. Christiansen, 1993. Growth and grazing control of abundance of the marine macroalga, Ulva lactuca L. in a eutrophic Danish estuary. Aquatic Botany 46: 101–109.

    Article  Google Scholar 

  • Granger, S. L., J. Mark, B. A. Buckley & M. Schwartz, 2000. An assessment of eutrophication in Greenwich Bay. In Schwartz, M. (ed.), Restoring Water Quality in Greenwich Bay: A Whitepaper Series, Vol. 1. Rhode Island Sea Grant, Narragansett, RI.

    Google Scholar 

  • Gruner, D., J. E. Smith, E. Seabloom, S. A. Sandin, J. T. Ngai, H. Hillebrand, W. Harpole, J. J. Elser, E. Cleland, M. E. S. Bracken, E. Borer & B. M. Bolker, 2008. A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecology Letters 11: 740–755.

    Article  PubMed  Google Scholar 

  • Guidone, M. & C. S. Thornber, 2013. Examination of Ulva bloom species richness and relative abundance reveals two cryptically co-occurring bloom species in Narragansett Bay, Rhode Island. Harmful Algae 24: 1–9.

    Article  Google Scholar 

  • Guidone, M., C. Thornber & E. Field, 2010. Snail grazing facilitates growth of a bloom-forming alga. Marine Ecology Progress Series 420: 83–89.

    Article  Google Scholar 

  • Guidone, M., C. S. Thornber & E. Vincent, 2012. Snail grazing facilitates growth of two morphologically similar bloom-forming Ulva species through different mechanisms. Journal of Ecology 100: 1105–1112.

    Article  Google Scholar 

  • Guidone, M., C. Thornber, B. Wysor & C. J. O’Kelly, 2013. Molecular and morphological diversity of Narragansett Bay (RI, USA) Ulva (Ulvales, Chlorophyta) populations. Journal of Phycology 49: 979–995.

    CAS  Google Scholar 

  • Hauxwell, J., J. McClelland, P. J. Behr & I. Valiela, 1998. Relative importance of grazing and nutrient controls of macroalgal biomass in three temperate shallow estuaries. Estuaries 21: 347–360.

    Article  Google Scholar 

  • Hauxwell, J., J. Cebrián, C. Furlong & I. Valiela, 2001. Macroalgal canopies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems. Ecology 82: 1007–1022.

    Article  Google Scholar 

  • Hillebrand, H., D. Gruner, E. Borer, M. E. S. Bracken, E. Cleland, J. J. Elser, W. Harpole, J. Ngai, E. Seabloom, J. Shurin & J. E. Smith, 2007. Consumer versus resource control of producer diversity depends on ecosystem type and producer community structure. Proceedings of the National Academy of Sciences USA 104: 10904–10909.

    Article  CAS  Google Scholar 

  • Hofmann, L., J. Nettleton, C. Neefus & A. Mathieson, 2010. Cryptic diversity of Ulva (Ulvales, Chlorophyta) in the Great Bay Estuarine System (Atlantic USA): introduced and indigenous distromatic species. European Journal of Phycology 45: 230–239.

    Article  Google Scholar 

  • Horne, A., J. McClelland & I. Valiela, 1994. The growth and consumption of macroalgae in estuaries: the role of invertebrate grazers along a nutrient gradient in Waquoit Bay, Massachusetts. Biological Bulletin 187: 279–280.

    Google Scholar 

  • Jormalainen, V., T. Honkanen, R. Koivikko & J. Eränen, 2003. Induction of phlorotannin production in a brown alga: defense or resource dynamics? Oikos 103: 640–650.

    Article  CAS  Google Scholar 

  • Kamermans, P., E. J. Malta, J. M. Verschuure, L. Schrijvers, L. F. Lentz & A. T. A. Lien, 2002. Effect of grazing by isopods and amphipods on growth of Ulva spp. (Chlorophyta). Aquatic Ecology 36: 425–433.

    Article  Google Scholar 

  • Karsten, U., C. Wiencke & G. Kirst, 1991. Growth pattern and beta-dimethylsulfoniopropionate (DMSP) content of marine macroalgae at different irradiances. Marine Biology 108: 151–155.

    Article  CAS  Google Scholar 

  • Karsten, U., C. Wiencke & G. O. Kirst, 1992. Dimethylsulfoniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature. Polar Biology 12: 603–607.

    Article  Google Scholar 

  • Korpinen, S., V. Jormalainen & T. Honkanen, 2007. Effects of nutrients, herbivory, and depth on the macroalgal community in the rocky sublittoral. Ecology 88: 839–852.

    Article  CAS  PubMed  Google Scholar 

  • Littler, M. M., D. S. Littler & P. R. Taylor, 1995. Selective herbivore increases biomass of its prey: a chiton–coralline reef-building association. Ecology 76: 1666–1681.

    Article  Google Scholar 

  • Lotze, H. K. & B. Worm, 2000. Variable and complementary effects of herbivores on different life stages of bloom-forming macroalgae. Marine Ecology Progress Series 200: 167–175.

    Article  Google Scholar 

  • Lyons, D., R. Scheibling & K. L. Van Alstyne, 2010. Spatial and temporal variation in DMSP content in the invasive seaweed Codium fragile ssp. fragile: effects of temperature, light, and grazing. Marine Ecology Progress Series 417: 51–61.

    Article  Google Scholar 

  • McLenaghan, N., A. Tyler, U. Mahl, R. Howarth & R. Marino, 2011. Benthic macroinvertebrate functional diversity regulates nutrient and algal dynamics in a shallow estuary. Marine Ecology Progress Series 426: 171–184.

    Article  CAS  Google Scholar 

  • Morgan, J. A., A. B. Aguiar, S. Fox, M. Teichberg & I. Valiela, 2003. Relative influence of grazing and nutrient supply on growth of the green macroalga Ulva lactuca in estuaries of Waquoit Bay, Massachusetts. Biological Bulletin 205: 252–253.

    Article  CAS  PubMed  Google Scholar 

  • Neckles, H., R. Wetzel & R. Orth, 1993. Relative effects of nutrient enrichment and grazing on epiphyte–macrophyte (Zostera marina L.) dynamics. Oecologia 93: 285–295.

    Article  Google Scholar 

  • Nelson, T. A., K. Haberlin, A. V. Nelson, H. Ribarich, R. Hotchkiss, K. L. Van Alstyne, L. Buckingham, D. J. Simunds & K. Fredrickson, 2008. Ecological and physiological controls of species composition in green macroalgal blooms. Ecology 89: 1287–1298.

    Article  PubMed  Google Scholar 

  • Nicotri, M. E., 1980. Factors involved in herbivore food preference. Journal of Experimental Marine Biology and Ecology 42: 13–26.

    Article  Google Scholar 

  • Norkko, J., E. Bonsdorff & A. Norkko, 2000. Drifting algal mats as an alternative habitat for benthic invertebrates: species specific responses to a transient resource. Journal of Experimental Marine Biology and Ecology 248: 79–104.

    Article  PubMed  Google Scholar 

  • Oczkowski, A. J., S. W. Nixon, K. Henry, P. DiMilla, M. Pilson, S. L. Granger, B. Buckley, C. Thornber, R. A. McKinney & J. Chaves, 2008. Distribution and trophic importance of anthropogenic nitrogen in Narragansett Bay: an assessment using stable isotopes. Estuaries Coasts 31: 53–69.

    Article  CAS  Google Scholar 

  • Råberg, S. & L. Kautsky, 2008. Grazer identity is crucial for facilitating growth of the perennial brown alga Fucus vesiculosus. Marine Ecology Progress Series 361: 111–118.

    Article  Google Scholar 

  • Russell, B. D. & S. D. Connell, 2007. Response of grazers to sudden nutrient pulses in oligotrophic versus eutrophic conditions. Marine Ecology Progress Series 349: 73–80.

    Article  Google Scholar 

  • Sala, N. M., M. D. Bertness & B. R. Silliman, 2008. The dynamics of bottom–up and top–down control in a New England salt marsh. Oikos 117: 1050–1056.

    Article  Google Scholar 

  • Shurin, J. B., E. Borer, E. W. Seabloom, K. Anderson, C. A. Blanchette, B. Broitman, S. Cooper & B. S. Halpern, 2002. A cross-ecosystem comparison of the strength of trophic cascades. Ecology Letters 5: 785–791.

    Article  Google Scholar 

  • Sly, E. 2013. Dietary contribution of polychlorinated biphenyl contaminated Ulva to Fundulus heteroclitus in the New Bedford Harbor, MA, Superfund site. M.S. Thesis, Northeastern University.

  • Steneck, R. S. & M. N. Dethier, 1994. A functional group approach to the structure of algal-dominated communities. Oikos 69: 476–498.

    Article  Google Scholar 

  • Svensson, C. J., S. Baden, P.-O. Moksnes & P. Åberg, 2012. Temporal mismatches in predator-herbivore abundance control algal blooms in nutrient-enriched seagrass ecosystems. Marine Ecology Progress Series 471: 61–71.

    Article  Google Scholar 

  • Thornber, C. S., E. Jones & J. J. Stachowicz, 2008. Differences in herbivore feeding preferences across a vertical rocky intertidal gradient. Marine Ecology Progress Series 363: 51–62.

    Article  Google Scholar 

  • Valiela, I., J. McClelland, J. Hauxwell, P. J. Behr, D. Hersh & K. Foreman, 1997. Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnology and Oceanography 42: 1105–1118.

    Article  Google Scholar 

  • Van Alstyne, K. L. & L. T. Houser, 2003. Dimethylsulfide release during macroinvertebrate grazing and its role as an activated chemical defense. Marine Ecology Progress Series 250: 175–181.

    Article  Google Scholar 

  • Van Alstyne, K. L., G. V. Wolfe, T. L. Freidenburg, A. Neill & C. Hicken, 2001. Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage. Marine Ecology Progress Series 213: 53–65.

    Article  Google Scholar 

  • Van Alstyne, K. L., L. Koellermeier & T. Nelson, 2007. Spatial variation in dimethylsulfoniopropionate (DMSP) production in Ulva lactuca (Chlorophyta) from the Northeast Pacific. Marine Biology 150: 1127–1135.

    Article  Google Scholar 

  • Van Alstyne, K. L., K. N. Pelletreau & A. Kirby, 2009. Nutritional preferences override chemical defenses in determining food choice by a generalist herbivore, Littorina sitkana. Journal of Experimental Marine Biology and Ecology 379: 85–91.

    Article  Google Scholar 

  • Vermeij, M. J. A., M. L. Dailer, S. M. Walsh, M. K. Donovan & C. M. Smith, 2010. The effects of trophic interactions and spatial competition on algal community composition on Hawaiian coral reefs. Marine Ecology 31: 291–299.

    Article  Google Scholar 

  • Williams, S. L. & M. H. Ruckelshaus, 1993. Effects of nitrogen availability and herbivory on eelgrass (Zostera marina) and epiphytes. Ecology 74: 904–918.

    Article  Google Scholar 

  • Worm, B. & H. K. Lotze, 2006. Effects of eutrophication, grazing, and algal blooms on rocky shores. Limnology and Oceanography 51: 569–579.

    Article  Google Scholar 

  • Yarrington, C. S., A. C. Tyler & A. H. Altieri, 2013. Do snails facilitate bloom-forming macroalgae in a eutrophic estuary? Journal of Experimental Marine Biology and Ecology 446: 253–261.

    Article  Google Scholar 

Download references

Acknowledgments

We thank C. Newton, N. Rohr, L. Steele, and two anonymous reviewers for their helpful comments that improved this manuscript. Additional thanks to J. Burkhardt, K. Eldredge, C. Newton, E. Vincent, and A. Viveiros for their help with cage deployment and sample processing, A. Barbosa, E. Blair, C. Donahue, K. Hyman, S. Rinehart, and N. Rohr for sample processing assistance, and E. Baker for his assistance with the University of Rhode Island Center for Marine Life Science facilities. Field experiments were conducted under Rhode Island Coastal Resources Management Council permit #s 2008-06-093, 2008-06-094, and 2008-06-095. Funding for this research was provided by Bay Window (the National Oceanic Atmospheric Administration), Rhode Island Sea Grant, the National Science Foundation (NSF IOB-0090825), the Sounds Conservancy Quebec-Labrador Foundation, and the University of Rhode Island. This material is also based upon work conducted at the Rhode Island Experimental Program to Stimulate Competitive Research (EPSCoR) supported Center for Marine Life Science that is supported by the National Science Foundation under EPSCoR Grant #1004057.

Author information

Author notes

  1. Michele Guidone

    Present address: Department of Biology, Armstrong State University, Savannah, GA, 31419, USA

Authors and Affiliations

  1. Department of Biological Sciences, University of Rhode Island, Kingston, RI, 02881, USA

    Michele Guidone & Carol S. Thornber

  2. Shannon Point Marine Center, Western Washington University, Anacortes, WA, 98221, USA

    Kathryn L. Van Alstyne

Authors
  1. Michele Guidone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carol S. Thornber
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kathryn L. Van Alstyne
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michele Guidone.

Additional information

Handling editor: Jonne Kotta

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 367 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guidone, M., Thornber, C.S. & Van Alstyne, K.L. Herbivore impacts on two morphologically similar bloom-forming Ulva species in a eutrophic bay. Hydrobiologia 753, 175–188 (2015). https://doi.org/10.1007/s10750-015-2204-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2204-6

Keywords

Search

Navigation