Historical Trends of Benthic Invertebrate Biodiversity Spanning 182 Years in a Southern New England Estuary
Benthic invertebrates support numerous ecosystem functions and services including shellfish production, energy flow to fishes, and biogeochemical cycles. The decline of marine biodiversity worldwide has raised concerns about effects on ecosystems. To examine biodiversity trends of Narragansett Bay over time, a list was compiled of all benthic invertebrate species collected from the bay since 1834. The list covers 104 studies spanning 182 years and currently holds 1214 unique taxa from 21 phyla, the majority of all animal phyla on Earth. A permuted estimator of number of species suggested there are about 300 more yet to be discovered. Widely varying sampling gear and sieve mesh sizes precluded the use of abundance data. Instead, multidimensional scaling and taxonomic distinctness were used with presence-absence data to examine biodiversity trends. The changes in community composition and decline of benthic biodiversity (p < 0.01) since 1855 are what would be expected of a community that gradually deteriorated in the face of increasing anthropogenic stressors. Taxonomic distinctness had negative correlations (p < 0.05) with human population in the watershed, total nitrogen inputs, and inputs of metals. This loss of benthic biodiversity has implications for ecosystem functions and services. As some of the stressors waned in the last two or three decades, following passage of environmental legislation in the 1970s, biodiversity appeared to show a partial recovery. An inventory of species, how it has changed over time, and understanding what caused those changes are important for assessing whether remediation programs are achieving improved water quality and ecosystem health.
KeywordsMarine benthic invertebrates Biodiversity Taxonomic distinctness Historical trends Narragansett Bay
We are grateful to Sheldon Pratt of the Graduate School of Oceanography at the University of Rhode Island (GSO-URI) who over many years has been an unparalleled fount of data and information on the Narragansett Bay benthos. Eric Lazo-Wasem and Lourdes Rojas at the Yale-Peabody Museum of Natural History, Patrick Randall at the Harvard Museum of Comparative Zoology, and William Moser at the Smithsonian’s National Museum of Natural History provided expert assistance with the historical data and access to their online databases was invaluable. Katherinne Duffy and Steven Lubar of Brown University provided information on the “Lost Museum.” The availability of historical books and reports from the Biodiversity Heritage Library was essential to our task. We are grateful for the assistance of Joyce Downey at Pell Marine Science Library, Hope Lappen at Brown University Library, David Remsen at Marine Biological Laboratory-Woods Hole Oceanographic Institution Library, and Dale Sheehy at the USEPA Atlantic Ecology Division library. We thank Deborah French McCay and Melanie Schroeder of Applied Science Associates, Inc. for providing the Mount Hope Bay data from MRI and the Weaver Cove LNG project. Also thanks to Candace Oviatt (GSO-URI) for providing the Marine Ecosystems Research Laboratory data and to Jeremy Collie (GSO-URI) for making available the invertebrate data from the bottom trawl time series. Review comments by Jeff Frithsen, Niels Hobbs, Anne Kuhn, and two anonymous reviewers improved the manuscript. This is contribution number ORD-023968 of the US Environmental Protection Agency, Office of Research and Development, National Health and Environmental Effects Research Laboratory, Atlantic Ecology Division, Narragansett, RI.
This article has not been subjected to review by the U.S. Environmental Protection Agency and does not necessarily reflect the views of the agency. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.
- Agassiz, A. 1865. North American Acalephae. Cambridge: Museum of Comparative Zoology at Harvard College.Google Scholar
- Barnes, E.W. 1906. A preliminary list of the marine Mollusca of Rhode Island. Annual Report of the Rhode Island Commissioners of Inland Fisheries 36: 30–37. Providence, R.I.Google Scholar
- BART [Bay Assessment & Response Team]. 2017. Rhode Island Department of Environmental Management. www.dem.ri.gov/programs/emergencyresponse/bart/latest.php. Accessed 1 August 2017.
- Biodiversity Heritage Library. 2017. http://www.biodiversitylibrary.org/. Accessed 15 Oct 2016.
- Boothman, W.S., and L. Coiro. 2017. Modern history of hypoxia in Narragansett Bay: the geochemical record. [abstract]. Coastal and Estuarine Research Federation conference, Providence, RI. November 2017.Google Scholar
- Callaway, R. 2016. Historical data reveal 30-year persistence of benthic fauna associations in heavily modified waterbody. Frontiers in Marine Science 3. https://doi.org/10.3389/fmars.2016.00141.
- Chintala, M., S.G. Ayvazian, W. Boothman, G. Cicchetti, L. Coiro, J. Copeland, et al. 2015. Trend analysis of stressors and ecological responses, particularly nutrients, in the Narragansett Bay watershed. U.S. Environmental Protection Agency, Narragansett, RI, USA.Google Scholar
- Clarke, K.R., R.N. Gorley, P.J. Somerfield, and R.M. Warwick. 2014. Change in marine communities: An approach to statistical analysis and interpretation. 3rd ed. Ivybridge, Devon: PRIMER-E Ltd.Google Scholar
- Desbonnet, A., and V. Lee. 1991. Historical trends: water quality and fisheries, Narragansett Bay. Narragansett: Rhode Island Sea Grant, University of Rhode Island.Google Scholar
- Dimitriadis, C., and D. Koutsoubas. 2011. Functional diversity and species turnover of benthic invertebrates along a local environmental gradient induced by an aquaculture unit: the contribution of species dispersal ability and rarity. Hydrobiologia 670 (1): 307–315. https://doi.org/10.1007/s10750-011-0668-6.CrossRefGoogle Scholar
- Dornelas, M., L.H. Antão, F. Moyes, A.E. Bates, A.E. Magorra, D. Adam, et al. (in press). BioTIME: a database of biodiversity time series for the Anthropocene. Global Ecology and Biogeography.Google Scholar
- EMAP [Environmental Monitoring and Assessment Program]. 2017. Office of Research and Development, U.S. Environmental Protection Agency. https://archive.epa.gov/emap/archive-emap/web/html/index-149.html. Accessed 15 Dec 2016.
- Fautin, D., P. Dalton, L.S. Incze, J.C. Leong, C. Pautzke, A. Rosenberg, et al. 2010. An overview of marine biodiversity in United States waters. PLoS One 5 (e11914): 1–47.Google Scholar
- Fewkes, J.W. 1881. Studies of the Jelly-fishes of Narragansett Bay. Bulletin of the Museum of Comparative Zoology, Harvard University in Cambridge 8 (8):141–182.Google Scholar
- Frithsen, J.B. 1989. The benthic communities within Narragansett Bay. An assessment completed for the Narragansett Bay Project, Report #NBP-90-28. Marine Ecosystems Research Laboratory, Graduate School of Oceanography, University of Rhode Island, Narragansett, RI.Google Scholar
- Gray, J.S., and M. Elliott. 2009. Ecology of marine sediments: from science to management. Oxford: Oxford University Press. 225 p.Google Scholar
- Hale, S.S., J.F. Paul, and J.F. Heltshe. 2004. Watershed landscape indicators of estuarine benthic condition. Estuaries 27: 284–296.Google Scholar
- Hale, S.S., M.M. Hughes, and H.W. Buffum. 2018. A database of historical benthic invertebrate biodiversity spanning 182 years in Narragansett Bay (Rhode Island and Massachusetts). U.S. Environmental Protection Agency, Office of Research and Development, Atlantic Ecology Division, Narragansett, RI. https://doi.org/10.23719/1429305.
- Harvard Museum of Comparative Zoology. 2017. MCZ Collections Database. www.mcz.harvard.edu/Departments/InvertZoo. Accessed 15 March 2017.
- Hobbs, N.-V., E. Lazo-Wasem, M. Faasse, J.R. Cordell, J.W. Chapman, C.S. Smith, R. Prezant, R. Shell, and J.T. Carlton. 2015. Going global: the introduction of the Asian isopod Ianiropsis serricaudis Gurjanova (Crustacea: Peracarida) to North America and Europe. Aquatic Invasions 10 (2): 177–187. https://doi.org/10.3391/ai.2015.10.2.06.CrossRefGoogle Scholar
- Imperial, M., D. Robadue, T. Hennessy, and M. Amaral. 2017. Retrospective governance analysis for the Narragansett Bay: analysis of governance response to ecosystem change in the Narragansett Bay watershed. Lighthouse Consulting Group, Warren, RI. Report for U.S. Environmental Protection Agency, Atlantic Ecology Division, Narragansett, R.I.Google Scholar
- ITIS [Integrated Taxonomic Information System]. 2017. http://www.itis.gov. Accessed 15 Sep 2016.
- Jeon, H., and C.A. Oviatt. 1991. A review of biological effects of toxic contaminants on organisms in Narragansett Bay. Narragansett Bay Estuary Program #NBP-91-75, Providence, R.I.Google Scholar
- Kemp, W.M., W.R. Boynton, J.E. Adolf, D.F. Boesch, W.C. Boicourt, G. Brush, J.C. Cornwell, T.R. Fisher, P.M. Glibert, J.D. Hagy, L.W. Harding, E.D. Houde, D.G. Kimmel, W.D. Miller, R.I.E. Newell, M.R. Roman, E.M. Smith, and J.C. Stevenson. 2005. Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Marine Ecology Progress Series 303: 1–29. https://doi.org/10.3354/meps303001.CrossRefGoogle Scholar
- King, J.W., J.B. Hubeny, C.L. Gibson, E. Laliberte, K.H. Ford, M. Cantwell, R. McKinney, P. Appleby 2008. Anthropogenic eutrophication of Narragansett Bay: evidence from dated sediment cores. In Science for ecosystem-based management: Narragansett Bay in the 21st Century, eds. A. Desbonnet and B.A. Costa-Pierce, 211–232. New York: Springer, DOI: https://doi.org/10.1007/978-0-387-35299-2_7.
- Kutcher, T.E. 2009. Human impacts on Narragansett Bay. In An Ecological Profile of the Narragansett Bay National Estuarine Research Reserve, ed. K.V. Raposa and M.L. Schwartz, 147–162. Narragansett: Rhode Island Sea Grant.Google Scholar
- Leidy, J. 1855. Contributions toward a knowledge of the marine invertebrate fauna of the coasts of Rhode Island and New Jersey. Journal of the Academy of Natural Sciences of Philadelphia 3: 1–20.Google Scholar
- Levin, L.A., D.F. Boesch, A. Covich, C. Dahm, C. Erséus, K.C. Ewel, R.T. Kneib, A. Moldenke, M.A. Palmer, P. Snelgrove, D. Strayer, and J.M. Weslawski. 2001. The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems 4 (5): 430–451. https://doi.org/10.1007/s10021-001-0021-4.CrossRefGoogle Scholar
- Louzao, M., N. Anadon, J. Arrontes, C. Alvarez-Claudio, D.M. Fuente, F. Ocharan, et al. 2010. Historical macrobenthic community assemblages in the Aviles Canyon, N Iberian Shelf: baseline biodiversity information for a marine protected area. Journal of Marine Systems 80 (1–2): 47–56. https://doi.org/10.1016/j.jmarsys.2009.09.006.CrossRefGoogle Scholar
- McMaster, R.L. 1960. Sediments of Narragansett Bay system and Rhode Island Sound, Rhode Island. Journal of Sedimentary Petrology 30: 249–274.Google Scholar
- Mead, A.D. 1899. The investigation of the plague which destroyed multitude of fish and Crustacea during the fall of 1898. Annual Report of the Rhode Island Commissioners of Inland Fisheries 29:31–34. Providence, R.I.Google Scholar
- Murray, D.W., W.L. Prell, C.E. Rincon, and E. Saarman. 2007. Physical property and chemical characteristics of surface grab samples from Narragansett Bay and the Providence and Seekonk Rivers, a summary of the Brown University Narragansett Bay Sediment Project (BUNBSP). Narragansett Bay Estuary Program, NBEP-2007-127, Providence, RI.Google Scholar
- NBC [Narragansett Bay Commission]. 2017. www.narrabay.com. Accessed 1 Feb 2017.
- NBEP [Narragansett Bay Estuary Program]. 2017. State of Narragansett Bay and its Watershed. Technical Report, Providence, RI. http://nbep.org/the-state-of-our-watershed/ Accessed 15 Sep 2017.
- NCA [National Coastal Assessment]. 2017. Office of Research and Development, U.S. Environmental Protection Agency, Washington, DC. https://archive.epa.gov/emap/archive-emap/web/html/index-149.html Accessed 1 Nov 2016.
- NCCA [National Coastal Condition Assessment]. 2017. Office of Water, U.S. Environmental Protection Agency, Washington, DC. http://water.epa.gov/type/oceb/assessmonitor/ncca.cfm Accessed 1 Feb 2017.
- Nixon, S.W. 1989. An extraordinary red tide and fish kill in Narragansett Bay. In Novel phytoplankton blooms: causes and impacts of recurrent brown tides and other unusual blooms, ed. E.M. Cosper, V.M. Bricelj, and E.J. Carpenter, 429–447. New York: Springer-Verlag.Google Scholar
- Nixon, S.W. 1990. A history of metal inputs to Narragansett Bay. Final report submitted to Narragansett Bay Project. Graduate School of Oceanography, University of Rhode Island, Narragansett, RI.Google Scholar
- Nixon, S.W. 1991. Recent metal inputs to Narragansett Bay. Narragansett Bay Project #NBP-91-52. Graduate School of Oceanography, University of Rhode Island, Narragansett, RI.Google Scholar
- Nixon, S.W., C.A. Oviatt, and S.S. Hale. 1976. Nitrogen regeneration and the metabolism of coastal marine bottom communities. In The role of terrestrial and aquatic organisms in decomposition processes, ed. J.M. Anderson and A. Macfadyen, 269–283. Oxford: Blackwell.Google Scholar
- Nixon, S.W., B.A. Buckley, S.L. Granger, L.A. Harris, A.J. Oczkowski, R.W. Fulweiler, and L.W. Cole. 2008. Nitrogen and phosphorus inputs to Narragansett Bay: past, present, and future. In Science for ecosystem-based management: Narragansett Bay in the 21st century, ed. A. Desbonnet and B.A. Costa-Pierce, 101–175. New York: Springer. https://doi.org/10.1007/978-0-387-35299-2_5.CrossRefGoogle Scholar
- OBIS [Ocean Biogeographic Information System]. 2017. http://www.iobis.org/. Accessed 15 June 2016.
- Obst, M., S. Vicario, K. Lundin, M. Berggren, A. Karlsson, R. Haines, et al. 2017. Marine long-term biodiversity assessment suggests loss of rare species in the Skagerrak and Kattegat region. Marine Biodiversity. https://doi.org/10.1007/s12526-017-0749-5.
- Olsen, S., D.D. Robadue, and V. Lee. 1980. An interpretive atlas of Narragansett Bay. Coastal Resources Center, University of Rhode Island. Marine Bulletin 40.Google Scholar
- Palumbi, S.R., P.A. Sandifer, J.D. Allan, M.W. Beck, D.G. Fautin, M.J. Fogarty, B.S. Halpern, L.S. Incze, J.A. Leong, E. Norse, J.J. Stachowicz, and D.H. Wall. 2009. Managing for ocean biodiversity to sustain marine ecosystem services. Frontiers in Ecology and the Environment 7 (4): 204–211. https://doi.org/10.1890/070135.CrossRefGoogle Scholar
- Parker, R.H. 1975. The study of benthic communities: a model and a review. Elsevier Oceanography Series. 9. Amsterdam: Elsevier.Google Scholar
- Pelletier, M., K. Ho, M. Cantwell, M. Perron, K. Rocha, R.M. Burgess, R. Johnson, K. Perez, J. Cardin, and M.A. Charpentier. 2017. Diagnosis of potential stressors adversely affecting benthic invertebrate communities in Greenwich Bay, Rhode Island, USA. Environmental Toxicology and Chemistry 36 (2): 449–462. https://doi.org/10.1002/etc.3562.CrossRefGoogle Scholar
- Pesch, C.E., E.J. Shumchenia, M.A. Charpentier and M.C. Pelletier. 2012. Imprint of the past: ecological history of Greenwich Bay, Rhode Island. EPA 600/R-12/050. U.S. Environmental Protection Agency, Office of Research and Development, Atlantic Ecology Division, Narragansett, RI.Google Scholar
- Pratt, S.D. 1992. Benthos. In Habitat inventory/resource mapping for Narragansett Bay and associated coastline. Final Report, eds. D. French, H. Rines, Chapt. 4. Narragansett: Applied Science Associates.Google Scholar
- RIDEM [Rhode Island Department of Environmental Management]. 2003. The Greenwich Bay fish kill–August 2003: causes, impacts and responses. Rhode Island Department of Environmental Management, Providence, RI. www.dem.ri.gov/pubs/fishkill.pdf.
- Shojaei, M.G., L. Gutow, J. Dannheim, E. Rachor, A. Schrӧder, and T. Brey. 2016. Common trends in German Bight benthic macrofaunal communities: assessing temporal variability and the relative importance of environmental variables. Journal of Sea Research 107: 25–33. https://doi.org/10.1016/j.seares.2015.11.002.CrossRefGoogle Scholar
- Smithsonian National Museum of Natural History. 2017. Invertebrate Zoology Collections. http://collections.nmnh.si.edu/search/iz/ Accessed 20 Oct 2016.
- Snelgrove, P.V.R., T.H. Blackburn, P. Hutchings, D. Alongi, J.F. Grassle, H. Hummel, et al. 1997. The importance of marine biodiversity in ecosystem processes. Ambio 26: 578–583.Google Scholar
- Snelgrove, P.V.R., M.C. Austen, S.J. Hawkins, T.M. Illiffe, R.T. Kneib, L.A. Levin, et al. 2004. Vulnerability of marine sedimentary ecosystem services to human activities. In Sustaining biodiversity and ecosystem services in soils and sediments, ed. D.H. Wall, Chapt. 7. Washington, D.C.: Island Press.Google Scholar
- Solan, M., R.J. Aspden, and D.M. Paterson. 2012. Marine biodiversity and ecosystem functioning: frameworks, methodologies, and integration. Oxford: Oxford University Press. https://doi.org/10.1093/acprof:oso/9780199642250.001.0001.CrossRefGoogle Scholar
- Sumner, F.B., R.C. Osborn, and L.J. Cole. 1911. A biological survey of the waters of Woods Hole and vicinity. Part 1. Section I. Physical and zoological. Bulletin of the Bureau of Fisheries 31, Washington, DC.Google Scholar
- Sweet, A.W. 1915. A sanitary survey of the Seekonk River, Ph.D. thesis, Brown University, Providence, RI.Google Scholar
- Tanner, Z.L. 1880. Report on the construction and work in 1880 of the Fish Commission Steamer Fish-Hawk. U.S. Fish Commission, Washington, DC.Google Scholar
- Thurstan, R.H., L. McClenachan, L.B. Crowder, J.A. Drew, J.N. Kittinger, P.S. Levin, C.M. Roberts, and J.M. Pandolfi. 2015. Filling historical data gaps to foster solutions in marine conservation. Ocean & Coastal Management 115: 31–40. https://doi.org/10.1016/j.ocecoaman.2015.04.019.CrossRefGoogle Scholar
- Totten, J.G. 1834. Description of some new shells, belonging to the coast of New England. The American Journal of Sciences and Arts 26: 366–369.Google Scholar
- Totten, J.G. 1835. Description of some shells, belonging to the coast of New England. The American Journal of Sciences and Arts 28: 347–353.Google Scholar
- Tweedley, J.R., C.S. Hallett, R.M. Warwick, K.R. Clarke, and I.C. Potter. 2015a. The hypoxia that developed in a microtidal estuary following an extreme storm produced dramatic changes in the benthos. Marine and Freshwater Research. https://doi.org/10.1071/MF14216.
- USEPA. 2010. National Coastal Condition Assessment’s Quality Assurance Project Plan https://www.epa.gov/sites/production/files/2013-11/documents/ncca-qapp.pdf
- Verrill, A.E., and S.I. Smith 1874. The invertebrate animals of Vineyard Sound and the adjacent waters, with an account of the physical features of the region. Chapt. VIII in Baird, S.F. Report on the condition of the sea fisheries of the south coast of New England in 1871 and 1872. United States Commission of Fish and Fisheries, Washington, D.C.Google Scholar
- Warwick, R.M., and K.R. Clarke. 2001. Practical measures of marine biodiversity based on relatedness of species. Oceanography and Marine Biology: an Annual Review 39: 207–231.Google Scholar
- Weslawski, J.M., P.V.R. Snelgrove, L.A. Levin, M.C. Austen, R.T. Kneib, T.M. Illiffe, et al. 2004. Marine sedimentary biota as providers of ecosystem goods and services. In Sustaining biodiversity and ecosystem services in soils and sediments, ed. D.H. Wall, Chapt 4. Washington, D.C.: Island Press.Google Scholar
- Worm, B., E.B. Barbier, N. Beaumont, J.E. Duffy, C. Folke, B.S. Halpern, J.B.C. Jackson, H.K. Lotze, F. Micheli, S.R. Palumbi, E. Sala, K.A. Selkoe, J.J. Stachowicz, and R. Watson. 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314 (5800): 787–790. https://doi.org/10.1126/science.1132294.CrossRefGoogle Scholar
- WoRMS [World Register of Marine Species]. 2017. http://www.marinespecies.org. Accessed 15 Oct 2016.
- Yale Peabody Museum of Natural History. 2017. Invertebrate Zoology Collections. http://collections.peabody.yale.edu/search. Accessed 1 Oct 2016.