Skip to main content

Advertisement

SpringerLink
Log in

Habitat Primarily Structures Seagrass Epifaunal Communities: a Regional-Scale Assessment in the Chesapeake Bay

  • Special Issue: Seagrasses Tribute to Susan Williams
  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Epifaunal invertebrates play an important role in seagrass systems, both by grazing epiphytic algae from seagrass blades and by acting as a major food source for higher trophic levels. However, while many studies have described epifaunal community properties at small spatial scales (1–10 m2) and across very large gradients (from continental coastlines to the entire globe), few have examined regional-scale (100–1000 km2) patterns or, more importantly, disentangled the drivers of these patterns. Here, we synoptically sampled the epifaunal invertebrates of 16 sites dominated by eelgrass (Zostera marina) across the lower Chesapeake Bay estuary to describe differences in epifaunal community abundance, biomass, richness, and composition. We then used complementary spatial and environmental data to identify potential drivers of these patterns. We found no significant associations between any variable and epifaunal abundance or biomass, but differences in epifaunal species richness correlated most strongly with water temperature, and differences in community composition were best explained by seagrass cover and the biomass of algal resources. Further exploration revealed the relationship between cover and community structure was driven by three specific species of peracarid crustaceans. Furthermore, when only species with direct development were included in the analysis, geographic distance, rather than seagrass cover, became a significant predictor of community composition, suggesting that species with particular traits (i.e., direct developers) are more likely to be found closer together in space.

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

Similar content being viewed by others

Data Availability

All associated data and code are available at Dryad: https://doi.org/10.25338/B85D1J.

References

  • Andrews, Jay D. 1973. Effects of tropical storm Agnes on epifaunal invertebrates in Virginia estuaries. Chesapeake Science 14 (4): 223–234.

    Google Scholar 

  • Baden, S, and C. Boström. 2001. The leaf canopy of seagrass beds: Faunal community structure and function in a salinity gradient along the Swedish coast. In Ecological comparisons of sedimentary shores, 151st ed., 213–236.

  • Barbier, Edward B., Sally D. Hacker, Chris Kennedy, Evamaria W. Koch, Adrian C. Stier, and Brian R. Silliman. 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs 81 (2): 169–193.

    Google Scholar 

  • Beck, Michael W., Kenneth L. Heck, Kenneth W. Able, Daniel L. Childers, David B. Eggleston, Bronwyn M. Gillanders, Benjamin Halpern, et al. 2001. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates: A better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. BioScience 51: 633–641.

    Google Scholar 

  • Blake, Rachael E., and J. Emmett Duffy. 2010. Grazer diversity affects resistance to multiple stressors in an experimental seagrass ecosystem. Oikos 119 (10): 1625–1635.

    Google Scholar 

  • Boström, Christoffer, and Johanna Mattila. 1999. The relative importance of food and shelter for seagrass-associated invertebrates: A latitudinal comparison of habitat choice by isopod grazers. Oecologia 120 (1): 162–170.

    Google Scholar 

  • Boström, Christoffer, Anna Törnroos, and Erik Bonsdorff. 2010. Invertebrate dispersal and habitat heterogeneity: Expression of biological traits in a seagrass landscape. Journal of Experimental Marine Biology and Ecology 390 (2): 106–117.

    Google Scholar 

  • Braun-Blanquet, J. 1965. Plant sociology: the study of plant communities. New York and London: Hafner Publishing Company.

  • Caine, Edsel A. 1974. Comparative functional morphology of feeding in three species of caprellids (Crustacea, Amphipoda) from the northwestern Florida Gulf Coast. Journal of Experimental Marine Biology and Ecology 15 (1): 81–96.

    Google Scholar 

  • Caine, Edsel A. 1989. Relationship between wave activity and robustness of caprellid amphipods. Journal of Crustacean Biology 9 (3): 425–431.

    Google Scholar 

  • Caine, Edsel A. 1998. First case of caprellid amphipod-hydrozoan mutualism. Journal of Crustacean Biology 18 (2): 317–320.

    Google Scholar 

  • Carr, Lindsey A., Katharyn E. Boyer, and Andrew J. Brooks. 2011. Spatial patterns of epifaunal communities in San Francisco Bay eelgrass (Zostera marina) beds. Marine Ecology 32 (1): 88–103.

    Google Scholar 

  • Chust, Guillem, Ernesto Villarino, Anne Chenuil, Xabier Irigoien, Nihayet Bizsel, Antonio Bode, Cecilie Broms, et al. 2016. Dispersal similarly shapes both population genetics and community patterns in the marine realm. Scientific Reports 6: 1–12.

    Google Scholar 

  • Clements, William H., and Robert J. Livingston. 1984. Prey selectivity of the fringed filefish Monacanthus ciliatus (Pisces: Monacanthidae): Role of prey accessibility. Marine Ecology Progress Series 16: 291–295.

    Google Scholar 

  • Cowen, Robert K., and Su Sponaugle. 2009. Larval dispersal and marine population connectivity. Annual Review of Marine Science 1 (1): 443–466.

    Google Scholar 

  • De Caceres, Miguel, and Pierre Legendre. 2009. Associations between species and groups of sites: Indices and statistical inference. Ecology 90 (12): 3566–3574.

    Google Scholar 

  • Douglass, James G., James G. Douglass, Kristin E. France, Kristin E. France, J. Paul Richardson, and J. Emmett Duffy. 2010. Seasonal and interannual change in a Chesapeake Bay eelgrass community: Insights into biotic and abiotic control of community structure. Limnology and Oceanography 55 (4): 1499–1520.

    CAS  Google Scholar 

  • Douglass, James G., J. Emmett Duffy, Amanda C. Spivak, and J. Paul Richardson. 2007. Nutrient versus consumer control of community structure in a Chesapeake Bay eelgrass habitat. Marine Ecology Progress Series 348: 71–83.

    CAS  Google Scholar 

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

    Google Scholar 

  • Dufrêne, Marc, and Pierre Legendre. 1997. Species assemblages and indicator species: The need for a flexible asymmetrical approach. Ecological Monographs 67: 345–366.

    Google Scholar 

  • Edgar, Graham J. 1993. Measurement of the carrying capacity of benthic habitats using a metabolic-rate based index. Oecologia 95 (1): 115–121.

    CAS  Google Scholar 

  • Edgar, Graham J., and M. Aoki. 1993. Resource limitation and fish predation: Their importance to mobile epifauna associated with Japanese Sargassum. Oecologia 95 (1): 122–133.

    CAS  Google Scholar 

  • Edgar, Graham J. 1990. The use of the size structure of benthic macrofaunal communities to estimate faunal biomass and secondary production. Journal of Experimental Marine Biology and Ecology 137 (3): 195–214.

    Google Scholar 

  • Eklöf, Johan S., Christian Alsterberg, Jonathan N. Havenhand, Kristina Sundbäck, Hannah L. Wood, and Lars Gamfeldt. 2012. Experimental climate change weakens the insurance effect of biodiversity. Ecology Letters 15 (8): 864–872.

    Google Scholar 

  • Fredette, Thomas J., and Robert J. Diaz. 1986. Life history of Gammarus mucronatus say (Amphipoda: Gammaridae) in warm temperate estuarine habitats, York River, Virginia. Journal of Crustacean Biology 6 (1): 57–78.

    Google Scholar 

  • Goslee, Sarah C., and Dean L. Urban. 2007. The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22: 1–19.

    Google Scholar 

  • Hall, Margaret O., and Susan S. Bell. 1988. Response of small motile epifauna to complexity of epiphytic algae on seagrass blades. Journal of Marine Research 46 (3): 613–630.

    Google Scholar 

  • Hayduk, Jennifer L., Sally D. Hacker, Jeremy S. Henderson, and Fiona Tomas. 2019. Evidence for regional-scale controls on eelgrass (Zostera marina) and mesograzer community structure in upwelling-influenced estuaries. Limnology and Oceanography 64 (3): 1120–1134.

    Google Scholar 

  • Heck, Kenneth L., Tim J.B. Carruthers, Carlos M. Duarte, A. Randall Hughes, Gary Kendrick, Robert J. Orth, and Susan W. Williams. 2008. Trophic transfers from seagrass meadows subsidize diverse marine and terrestrial consumers. Ecosystems 11 (7): 1198–1210.

    Google Scholar 

  • Hovel, Kevin A., Mark S. Fonseca, D.L. Myer, W.J. Kenworthy, and P.E. Whitfield. 2002. Effects of seagrass landscape structure, structural complexity and hydrodynamic regime on macrofaunal densities in North Carolina seagrass beds. Marine Ecology Progress Series 243: 11–24.

    Google Scholar 

  • Janzen, Daniel H. 1970. Herbivores and the number of tree species in tropical forests. The American Naturalist 104 (940): 501–528.

    Google Scholar 

  • Jost, Lou. 2010. The relation between evenness and diversity. Diversity 2 (2): 207–232.

    Google Scholar 

  • Kinlan, Brian P., and Steven D. Gaines. 2003. Propagule dispersal in marine and terrestrial environments: A community perspective. Ecology 84 (8): 2007–2020.

    Google Scholar 

  • Lefcheck, Jonathan S., Brent B. Hughes, Andrew J. Johnson, Bruce W. Pfirrmann, Douglas B. Rasher, Ashley R. Smyth, Bethany L. Williams, Michael W. Beck, and Robert J. Orth. 2019. Are coastal habitats important nurseries? A meta-analysis. Conservation Letters 12: e12645.

    Google Scholar 

  • Lefcheck, Jonathan S., Scott R. Marion, Alfonso V. Lombana, and Robert J. Orth. 2016. Faunal communities are invariant to fragmentation in experimental seagrass landscapes. PLoS One 11 (5): e0156550.

    Google Scholar 

  • Lefcheck, Jonathan S., David J. Wilcox, Rebecca R. Murphy, Scott R. Marion, and Robert J. Orth. 2017. Multiple stressors threaten the imperiled coastal foundation species eelgrass (Zostera marina) in Chesapeake Bay, USA. Global Change Biology 23 (9): 3474–3483.

    Google Scholar 

  • Legendre, Pierre, François-Joseph Lapointe, and Philippe Casgrain. 1994. Modeling brain evolution from behavior: A permutational regression approach. Evolution 48 (5): 1487–1499.

    Google Scholar 

  • Lichstein, Jeremy W. 2007. Multiple regression on distance matrices: A multivariate spatial analysis tool. Plant Ecology 188 (2): 117–131.

    Google Scholar 

  • Main, Kevan L. 1985. The influence of prey identity and size on selection of prey by two marine fishes. Journal of Experimental Marine Biology and Ecology 88 (2): 145–152.

    Google Scholar 

  • Manley, Stephen R., Robert J. Orth, and Leonardo Ruiz-Montoya. 2015. Roles of dispersal and predation in determining seedling recruitment patterns in a foundational marine angiosperm. Marine Ecology Progress Series 533: 109–120.

    Google Scholar 

  • Marsh, G. Alex. 1973. The Zostera epifaunal community in the York River, Virginia. Chesapeake Science 14 (2): 87–97.

    Google Scholar 

  • McCain, John C. 1965. The Caprellidae (Crustacea: Amphipoda) of Virginia. Chesapeake Science 6 (3): 190–196.

    Google Scholar 

  • Micheli, Fiorenza, Melanie J. Bishop, Charles H. Peterson, and José Rivera. 2008. Alteration of seagrass species composition and function over two decades. Ecological Monographs 78 (2): 225–244.

    Google Scholar 

  • Momota, Kyosuke, and Masahiro Nakaoka. 2018. Seasonal change in spatial variability of eelgrass epifaunal community in relation to gradients of abiotic and biotic factors. Marine Ecology 39 (4): e12522.

    Google Scholar 

  • Moore, Althea F.P., and J. Emmett Duffy. 2016. Foundation species identity and trophic complexity affect experimental seagrass communities. Marine Ecology Progress Series 556: 105–121.

    Google Scholar 

  • Morales-Núñez, Andrés G., and Paulinus Chigbu. 2019. Abundance, distribution, and species composition of amphipods associated with macroalgae from shallow waters of the Maryland coastal bays, USA. Marine Biodiversity 49 (1): 175–191.

    Google Scholar 

  • Najjar, Raymond G., Christopher R. Pyke, Mary Beth Adams, Denise Breitburg, Carl Hershner, Michael Kemp, Robert Howarth, Margaret R. Mulholland, Michael Paolisso, David Secor, Kevin Sellner, Denice Wardrop, and Robert Wood. 2010. Potential climate-change impacts on the Chesapeake Bay. Estuarine, Coastal and Shelf Science 86 (1): 1–20.

    CAS  Google Scholar 

  • Nakaoka, Masahiro, Tetsuhiko Toyohara, and Masatoshi Matsumasa. 2001. Seasonal and between-substrate variation in mobile epifaunal community in a multispecific seagrass bed of Otsuchi Bay, Japan. Marine Ecology 22 (4): 379–395.

    Google Scholar 

  • Namba, Mizuho, Marina Hashimoto, Minako Ito, Kyosuke Momota, Carter Smith, Takefumi Yorisue, and Masahiro Nakaoka. 2020. The effect of environmental gradient on biodiversity and similarity of invertebrate communities in eelgrass (Zostera marina) beds. Ecological Research 35 (1): 61–75.

    Google Scholar 

  • Neckles, Hilary A., Richard L. Wetzel, and Robert J. Orth. 1993. Relative effects of nutrient enrichment and grazing on epiphyte-macrophyte (Zostera marina L.) dynamics. Oecologia 93 (2): 285–295.

    Google Scholar 

  • Nelson, W.G., and R.W. Virnstein. 1997. Long-term dynamics of seagrass macrobenthos: Asynchronous population variability in space and time. Oceanographic Literature Review 2: 140.

    Google Scholar 

  • Oksanen, Jari, F. Guillaume Blanchet, Michael Friendly, Roeland Kindt, Pierre Legendre, Dan McGlinn, and Peter R. Minchin, et al. 2018. Vegan: Community ecology package. R package version 2: 5–3 https://CRAN.R-project.org/package=vegan.

    Google Scholar 

  • Orth, Robert J., Tim J.B. Carruthers, William C. Dennison, Carlos M. Duarte, James W. Fourqurean, Kenneth L. Heck, A. Randall Hughes, et al. 2006. A global crisis for seagrass ecosystems. BioScience 56 (12): 987–996.

    Google Scholar 

  • Orth, Robert J., and Kenneth L. Heck. 1980. Structural components of eelgrass (Zostera marina) meadows in the lower Chesapeake Bay: Fishes. Estuaries 3 (4): 278–288.

    Google Scholar 

  • Orth, Robert J., Kenneth L. Heck, and Jacques van Montfrans. 1984. Faunal communities in seagrass beds: A review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7 (4): 339–350.

    Google Scholar 

  • Orth, Robert J., and Jacques Van Montfrans. 1984. Epiphyte-seagrass relationships with an emphasis on the role of micrograzing: A review. Aquatic Botany 18 (1–2): 43–69.

    Google Scholar 

  • Palmer, Margaret A., J. David Allan, and Cheryl Ann Butman. 1996. Dispersal as a regional process affecting the local dynamics of marine and stream benthic invertebrates. Trends in Ecology & Evolution 11 (8): 322–326.

    CAS  Google Scholar 

  • Parker, John D., J. Emmett Duffy, and Robert J. Orth. 2001. Plant species diversity and composition: Experimental effects on marine epifaunal assemblages. Marine Ecology Progress Series 224: 55–67.

    Google Scholar 

  • Ralph, Gina M., Rochelle D. Seitz, Robert J. Orth, Kathleen E. Knick, and Romuald N. Lipcius. 2013. Broad-scale association between seagrass cover and juvenile blue crab density in Chesapeake Bay. Marine Ecology Progress Series 488: 51–63.

    Google Scholar 

  • Reed, Brendan J., and Kevin A. Hovel. 2006. Seagrass habitat disturbance: How loss and fragmentation of eelgrass Zostera marina influences epifaunal abundance and diversity. Marine Ecology Progress Series 326: 133–143.

    Google Scholar 

  • Reynolds, Pamela L., John J. Stachowicz, Kevin Hovel, Christoffer Boström, Katharyn Boyer, Mathieu Cusson, and Johan S. Eklöf, et al. 2018. Latitude, temperature, and habitat complexity predict predation pressure in eelgrass beds across the northern hemisphere. Ecology 99 (1): 29–35.

    Google Scholar 

  • Richardson, J. Paul, Jonathan S. Lefcheck, and Robert J. Orth. 2018. Warming temperatures alter the relative abundance and distribution of two co-occurring foundational seagrasses in Chesapeake Bay, USA. Marine Ecology Progress Series 599: 65–74.

    Google Scholar 

  • Rutherford, Scott, Steven D’Hondt, and Warren Prell. 1999. Environmental controls on the geographic distribution of zooplankton diversity. Nature 400 (6746): 749–753.

    CAS  Google Scholar 

  • Ryer, Clifford H. 1988. Pipefish foraging: Effects of fish size, prey size and altered habitat complexity. Marine Ecology Progress Series 48: 37–45.

    Google Scholar 

  • Sirota, L., and Ka Hovel. 2006. Simulated eelgrass Zostera marina structural complexity: Effects of shoot length, shoot density, and surface area on the epifaunal community of San Diego Bay, California, USA. Marine Ecology Progress Series 326: 115–131.

    Google Scholar 

  • Stark, Keila A., Patrick L. Thompson, Jennifer Yakimishyn, Lynn Lee, and Mary I. O’Connor. 2018. Beyond a single patch: local and regional processes explain biodiversity patterns in a seagrass epifaunal metacommunity. bioRxiv: 482406.

  • Stoner, Allan W. 1980. The role of seagrass biomass in the organization of benthic macrofaunal assemblages. Bulletin of Marine Science 30: 537–551.

    Google Scholar 

  • Thomsen, Mads S., Andrew H. Altieri, Christine Angelini, Melanie J. Bishop, Paul E. Gribben, Gavin Lear, Qiang He, David R. Schiel, Brian R. Silliman, Paul M. South, David M. Watson, Thomas Wernberg, and Gerhard Zotz. 2018. Secondary foundation species enhance biodiversity. Nature Ecology & Evolution 2 (4): 634–639.

    Google Scholar 

  • Thomson, Jordan A., Derek A. Burkholder, Michael R. Heithaus, James W. Fourqurean, Matthew W. Fraser, John Statton, and Gary A. Kendrick. 2015. Extreme temperatures, foundation species, and abrupt ecosystem change: An example from an iconic seagrass ecosystem. Global Change Biology 21 (4): 1463–1474.

    Google Scholar 

  • Unsworth, Richard K.F., Lina Mtwana Nordlund, and Leanne C. Cullen-Unsworth. 2019. Seagrass meadows support global fisheries production. Conservation Letters 12 (1): e12566.

    Google Scholar 

  • Valentine, John F., and J. Emmett Duffy. 2006. The central role of grazing in seagrass ecology. In Seagrasses: Biology, ecology and conservation, ed. Anthony W.D. Larkum, Robert J. Orth, and Carlos M. Duarte, 463–501. Dordrecht: Springer Netherlands.

    Google Scholar 

  • Vasseur, David A., John P. DeLong, Benjamin Gilbert, Hamish S. Greig, Christopher D.G. Harley, Kevin S. McCann, Van Savage, Tyler D. Tunney, and Mary I. O’Connor. 2014. Increased temperature variation poses a greater risk to species than climate warming. Proceedings of the Royal Society B: Biological Sciences 281 (1779): 20132612.

    Google Scholar 

  • Virnstein, Robert W. 1990. The large spatial and temporal biological variability of Indian River lagoon. Florida Scientist 53: 249–256.

    Google Scholar 

  • Virnstein, Robert W., Walter G. Nelson, F. Graham Lewis, and Robert K. Howard. 1984. Latitudinal patterns in seagrass epifauna: Do patterns exist, and can they be explained? Estuaries 7 (4): 310–330.

    Google Scholar 

  • Walsh, C.J., and B.D. Mitchell. 1998. Factors associated with variations in abundance of epifaunal caridean shrimps between and within estuarine seagrass meadows. Marine and Freshwater Research 49 (8): 769–777.

    Google Scholar 

  • Whippo, Ross, Nicole S. Knight, Carolyn Prentice, John Cristiani, Matthew R. Siegle, and Mary I. O’Connor. 2018. Epifaunal diversity patterns within and among seagrass meadows suggest landscape-scale biodiversity processes. Ecosphere 9 (11): e02490.

    Google Scholar 

  • Yamada, Katsumasa, Hori Masakazu, Tanaka Yoshiyuki, Hasegawa Natsuki, and Nakaoka Masahiro. 2007. Temporal and spatial macrofaunal community changes along a salinity gradient in seagrass meadows of Akkeshi-ko estuary and Akkeshi Bay, northern Japan. Hydrobiologia 592 (1): 345–358.

    Google Scholar 

  • Yeager, Lauren A., Julie K. Geyer, and Fredrick Joel Fodrie. 2019. Trait sensitivities to seagrass fragmentation across spatial scales shape benthic community structure. Journal of Animal Ecology 88 (11): 1743–1754. https://doi.org/10.1111/1365-2656.13067.

    Article  Google Scholar 

Download references

Acknowledgments

We thank the US Environmental Protection Agency’s Chesapeake Bay Program for the environmental data. We also thank Corey Holbert, Andrew Johnson, Paul Richardson, David Wilcox, Billy Storm, Justin Mitchell, and all the volunteers who helped with data collection and processing. Finally, we thank the two reviewers, Dr. Robert Virnstein and Dr. Masahiro Nakaoka, for their helpful comments on earlier versions of this manuscript. This is contribution no. 3961 of the Virginia Institute of Marine Science, William & Mary, and 61 from the Smithsonian’s MarineGEO and Tennenbaum Marine Observatories Network.

Funding

Funding for this work was from the Virginia Recreational Fishing License Fund administered by the Virginia Marine Resources Commission. JSL and CEM were supported by the Michael E. Tennenbaum Secretarial Scholar gift to the Smithsonian Institution.

Author information

Author notes

  1. Claire E. Murphy

    Present address: Department of Evolution and Ecology, University of California, Davis, CA, 95616, USA

Authors and Affiliations

  1. Tennenbaum Marine Observatories Network, MarineGEO, Smithsonian Institution, Edgewater, MD, 21037, USA

    Claire E. Murphy & Jonathan S. Lefcheck

  2. Department of Biological Sciences, Virginia Institute of Marine Science, Gloucester Point, VA, 23062, USA

    Claire E. Murphy & Robert J. Orth

  3. Department of Biology, The College of William & Mary, Williamsburg, VA, 23185, USA

    Claire E. Murphy

Authors
  1. Claire E. Murphy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert J. Orth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jonathan S. Lefcheck
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claire E. Murphy.

Additional information

Communicated by Melisa C. Wong

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Murphy, C.E., Orth, R.J. & Lefcheck, J.S. Habitat Primarily Structures Seagrass Epifaunal Communities: a Regional-Scale Assessment in the Chesapeake Bay. Estuaries and Coasts 44, 442–452 (2021). https://doi.org/10.1007/s12237-020-00864-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-020-00864-4

Keywords

Search

Navigation