Elsevier

Marine Pollution Bulletin

Volume 133, August 2018, Pages 77-87
Marine Pollution Bulletin

Six decades of change in pollution and benthic invertebrate biodiversity in a southern New England estuary

https://doi.org/10.1016/j.marpolbul.2018.05.019Get rights and content

Highlights

  • Benthic invertebrate biodiversity changes correlated with pollution indicators.

  • A mid-bay reference site showed moderate changes in community composition.

  • A site in urbanized upper bay showed significant decline in taxonomic distinctness.

  • Signs of biodiversity recovery were found as inputs of some stressors declined.

  • Taxonomic distinctness statistically independent of number of species in sample

Abstract

Pollution has led to a decline of benthic invertebrate biodiversity of Narragansett Bay, raising questions about effects on ecosystem functions and services including shellfish production, energy flow to fishes, and biogeochemical cycles. Changes in community composition and taxonomic distinctness (biodiversity) were calculated from the 1950s—when quantitative benthic invertebrate data first became available—to 2015. Change in community composition of the bay was correlated with changes in dissolved inorganic nitrogen, dissolved oxygen, and sediment contaminants. A mid-bay reference site showed moderate changes in community composition but no change in biodiversity. In contrast, a more impacted site in the upper bay showed substantial differences in community composition over time and a decline in taxonomic distinctness. Bay-wide, as inputs of some stressors such as nutrients and sediment contaminants have declined, there are signs of recovery of benthic biodiversity but other stressors such as temperature and watershed development are increasing.

Introduction

Biodiversity supports the functioning of ecosystems and the services they provide to people (Worm et al., 2006; Palumbi et al., 2009; Fautin et al., 2010; Solan et al., 2012; Goulletquer et al., 2014; Dornelas et al., in press). Ecosystem functions and services driven by benthic biodiversity include seafood for human consumption, water filtration (water quality), bioturbation and bio-irrigation (supporting nutrient cycling), shoreline protection, habitat for other species, and cultural services such as recreation (Snelgrove et al., 1997; Snelgrove, 1998, Snelgrove, 1999; Levin et al., 2001; Weslawski et al., 2004; Goulletquer et al., 2014).

Marine ecosystems around the world have experienced rapid declines in biodiversity as a result of multiple stressors (Snelgrove et al., 2004; Jackson, 2008; Worm et al., 2006; Fautin et al., 2010; McCauley et al., 2015) and quantifying these changes has been recognized as a crucial research need (Fautin et al., 2010; Dornelas et al., in press). Estuarine functions are affected when benthic species losses lead to less food available for fishes, fewer large bioturbators, fewer suspension feeders, loss of reef or mat habitat, or collapse of biological interactions (Goulletquer et al., 2014). Loss of rare species reduces ecosystem functioning, productivity, and the ability to respond to environmental perturbations (Micheli and Halpern, 2005; Mouillat et al., 2013; Obst et al., 2017). Long-term benthic community studies have contributed to an understanding of how the sum of multiple anthropogenic factors over long periods of time has adversely affected biodiversity. Factors implicated include eutrophication and hypoxia (Kemp et al., 2005; Pranovi et al., 2008; Reise et al., 2008; Krann et al., 2011), warming waters (Callaway et al., 2007; Shojaei et al., 2016), commercial fishing (Callaway et al., 2007; Trott, 2016), contaminants and combinations of these (Obst et al., 2017). Benthic communities are good integrators of these cumulative stressors (Obst et al., 2017).

This article describes how species biodiversity and community composition of the soft-bottom benthic invertebrate macrofaunal community of Narragansett Bay has changed over the past six decades and relates changes, where possible, to anthropogenic drivers. Sampling methods that allowed such quantitative comparisons of benthic invertebrates in the bay began in the 1950s. Recently, in an effort to reduce eutrophication and hypoxia, nutrient loads to the bay have been reduced, including a 50% reduction of total nitrogen input from wastewater treatment facilities (WWTF) that occurred 2005–2013 (NBEP, 2017). Additionally, inputs of metals, petroleum hydrocarbons, and synthetic organic contaminants have declined in recent years while other stressors (e.g., water temperature, watershed development) are increasing (NBEP, 2017). Questions arise as to what the effect will be on the estuarine ecosystem. This article explores whether it is possible to detect a benthic response to these changes.

Section snippets

Study area

Narragansett Bay is a temperate northeastern U.S. estuary in Rhode Island and Massachusetts located at the northern end of the Virginian Biogeographic Province (Fig. 1). Benthic invertebrate biodiversity in the bay stems from a mix of warm temperate species of the Virginian Province and Arctic-boreal species more common in the Acadian Biogeographic Province to the north (Hale, 2010), continental shelf species that extend up into the deep East Passage (Pratt, 1992), and rocky shore habitats at

Biodiversity status and trends for Narragansett Bay

The USEPA dataset spanning 25 years and 166 stations included 561 taxa. Five species dominated numerical abundance (Table 1, Fig. 2). Like other soft-bottom benthic studies (Gray and Elliott, 2009; Trott, 2016), most of the taxa in the USEPA study were rare, as shown by the long tail to the right in the species dominance plot (Fig. 2). Rare species (<20 occurrences in the 25-year dataset) comprised 88% of all taxa. Some of the species are rare because they were not efficiently captured by the

Current status of Narragansett Bay benthic communities

The mid-bay area has been characterized as a Nephtys-Nucula community (Pratt, 1992). In the USEPA 25-yr dataset for the entire bay, the bivalve Nucula proxima was in the top five for both prevalence and abundance but the polychaete Nephtys incisa was so only for prevalence. The polychaete Mediomastus ambiseta was more prevalent and abundant than both. Nucula spp. and M. ambiseta were the species contributing the most to community similarity in the entire bay in the 1990s and the 2000s. Thus,

Conclusions

For the entire bay (USEPA dataset) and for the North Jamestown site, ∆* showed a rising trend toward the end of each time series. Although not statistically significant, these trends may be indicative of a recovery of biodiversity in response to decreased anthropogenic stressors, as suggested by an analysis of historical data collected over 182 years (Hale et al., 2018a). Whether these trends will continue and become significant will require further years of monitoring. It was too early to

Acknowledgments

We thank Sheldon Pratt of the Graduate School of Oceanography at the University of Rhode Island (URI GSO) for many sources of data and discussions of the Narragansett Bay benthos. We are grateful to 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 (URI GSO) for the MERL data, to Jeremy Collie (URI GSO) for the invertebrate data from the GSO trawl time

References (97)

  • J.S. Collie et al.

    Long-term shifts in the species composition of a coastal fish community

    Can. J. Fish. Aquat. Sci.

    (2008)
  • A. D'Agostino et al.

    Infaunal Invertebrates in the Near Shore Waters of Long Island Sound

    (1973)
  • A. Desbonnet et al.

    Historical Trends: Water Quality and Fisheries

    (1991)
  • R.J. Diaz et al.

    Long-term trends of benthic habitats related to reduction in wastewater discharge to Boston Harbor

    Estuar. Coasts

    (2008)
  • C. Dimitriadis et al.

    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

    (2011)
  • M. Dornelas et al.

    BioTIME: a database of biodiversity time series for the Anthropocene

    Glob. Ecol. Biogeogr.

    (2018)
  • G. Ellis

    An Examination of the Benthic Macrofauna of Narragansett Bay and the Possible Implications of Winter-Spring Bloom Intensity on Population Size

    (2002)
  • EMAP [Environmental Monitoring and Assessment Program]

    Office of Research and Development

    (2017)
  • D. Fautin et al.

    An overview of marine biodiversity in United States waters

    PLoS ONE

    (2010)
  • D. French et al.

    Habitat Inventory/Resource Mapping for Narragansett Bay and Associated Coastline. Final Report Submitted to Narragansett Bay Project, Providence, RI

    (1992)
  • J.B. Frithsen

    The benthic communities within Narragansett Bay

  • P. Goulletquer et al.

    Biodiversity in the Marine Environment

    (2014)
  • J.S. Gray et al.

    Ecology of Marine Sediments

    (2009)
  • GSO [Graduate School of Oceanography]

    Fish Trawl Survey

    (2017)
  • S.S. Hale

    The Role of Benthic Communities in the Nutrient Cycles of Narragansett Bay

    (1974)
  • S.S. Hale

    Biogeographical patterns of marine benthic macroinvertebrates along the Atlantic coast of the northeastern USA

    Estuar. Coasts

    (2010)
  • S.S. Hale et al.

    Coastal ecological data from the Virginian Biogeographic Province, 1990–1993

    Ecology

    (2002)
  • S.S. Hale et al.

    Watershed landscape indicators of estuarine benthic condition

    Estuaries

    (2004)
  • S.S. Hale et al.

    Eutrophication and hypoxia diminish ecosystem functions of benthic communities in a New England estuary

    Front. Mar. Sci.

    (2016)
  • S.S. Hale et al.

    Subtidal benthic invertebrates moving north along the U.S. Atlantic coast

    Estuar. Coasts

    (2017)
  • S.S. Hale et al.

    Historical trends of benthic invertebrate biodiversity spanning 182 years in a southern New England estuary

    Estuar. Coasts

    (2018)
  • S.S. Hale et al.

    A Database of Historical Benthic Invertebrate Biodiversity Spanning 182 Years in Narragansett Bay (Rhode Island and Massachusetts)

    (2018)
  • ITIS [Integrated Taxonomic Information System]
  • J.B.C. Jackson

    Ecological extinction and evolution in the brave new ocean

    Proc. Natl. Acad. Sci.

    (2008)
  • H. Jeon et al.

    A review of biological effects of toxic pollutants on organisms in Narragansett Bay

  • W.M. Kemp et al.

    Eutrophication of Chesapeake Bay: historical trends and ecological interactions

    Mar. Ecol. Prog. Ser.

    (2005)
  • J. Kiddon et al.

    U.S. Environmental Protection Agency's National Coastal Assessment, Northeast, 2000–2006

  • C. Krahforst et al.

    An ecosystem-based perspective of Mount Hope Bay

  • C. Krann et al.

    Now an empty mudflat: past and present benthic abundances in the western Dutch Wadden Sea

    Helgol. Mar. Res.

    (2011)
  • L.A. Levin et al.

    The function of marine critical transition zones and the importance of sediment biodiversity

    Ecosystems

    (2001)
  • E.R. Long et al.

    Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments

    Environ. Manag.

    (1995)
  • D.G. MacDonald et al.

    Natural and anthropogenic influences on the Mount Hope Bay ecosystem: concluding remarks

    Northeast. Nat.

    (2006)
  • D.J. McCauley et al.

    Marine defaunation: animal loss in the global ocean

    Science

    (2015)
  • D.F. McCay et al.

    Characterization of the infaunal benthic macroinvertebrate assemblages of Mount Hope Bay and the lower Taunton River for the Weaver's Cove Offshore Berth Project

  • R.L. McMaster

    Sediments of Narragansett Bay system and Rhode Island Sound, Rhode Island

    J. Sediment. Petrol.

    (1960)
  • MERL [Marine Ecosystems Research Laboratory]

    Narragansett Bay benthic data sampling

  • F. Micheli et al.

    Low functional redundancy in coastal marine assemblages

    Ecol. Lett.

    (2005)
  • D. Mouillat et al.

    Rare species support vulnerable functions in high-diversity ecosystems

    PLoS Biol.

    (2013)
  • Cited by (8)

    • Macrobenthic community of a tropical bay system revisited: Historical changes in response to anthropogenic forcing

      2021, Marine Pollution Bulletin
      Citation Excerpt :

      Coastal eutrophication, organic enrichment, deoxygenation (Zhang et al., 2018; Rousi et al., 2019), and disrupted benthic-pelagic coupling (Agnetta et al., 2019) affect marine communities (Briggs et al., 2017). Gradual loss of species (Ehrnsten et al., 2019), composition, abundance, and biomass shift paradigms have far-reaching consequences not only on the ecosystem functioning (Rosenberg, 2014; McQuatters-gollop et al., 2019) but also on the blue economy (Hale et al., 2018). Macrobenthic organisms (or benthic macrofauna and/or benthic macroinvertebrates as used interchangeably in this study) that constitute a significant component of marine communities play a vital role in integrating sediment organic matter and nutrient regeneration and thereby facilitate benthic-pelagic coupling, marine food-web functioning, and ecosystem resilience (Herman et al., 1999; Li et al., 2017; Sinha et al., 2021).

    • Disentangling effects of river inflow and marine diffusion in shaping the planktonic communities in a heavily polluted estuary

      2020, Environmental Pollution
      Citation Excerpt :

      The gateway and linkage function of estuary between marine and freshwater systems is an essential feature of many invertebrates and vertebrates. Therefore, estuary is an important and complex environment with a high biodiversity value (Hale et al., 2018). Furthermore, the estuarine ecosystem is extremely sensitive because it is exposed to pressures from both the river and the sea.

    • Bottom-trawl catch composition in a highly polluted coastal area reveals multifaceted native biodiversity and complex communities of fouling organisms on litter discharge

      2020, Marine Environmental Research
      Citation Excerpt :

      The pairwise results showed no differences when contrasting both cotton versus nylon and cotton versus synthetic fiber, while the remaining pairwise comparisons exhibited significant differences (Supplementary Table 14). Most studies dealing with highly impacted coastal areas reported changes and declines in abundance and biomass in biological communities and strong habitat degradation, with successful remediation procedures resulting in a general return to unstressed conditions (e.g. Poland et al., 2003; Adams et al., 2005; Johnston and Roberts, 2009; Borja et al., 2011; Hale et al., 2018). Generalizations of such results are difficult due to natural variability among geographic areas, different sampling methods, and level of taxonomic expertise of the authors.

    • Novel hybrid methods applied for spatial prediction of mercury and variable selection of trace elements in coastal areas of USA

      2020, Marine Pollution Bulletin
      Citation Excerpt :

      The respective monitoring data were applied as a representative data set for statistical inference and spatial analysis in environmental sciences. Meanwhile, there have been multiple applications of this data set in earlier studies in environmental and ecological researches (e.g. Hale et al., 2018). A subsample of eleven trace elements including Aluminium (Al), Arsenic (As), Cadmium (Cd), Chromium (Cr), Copper (Cu), Iron (Fe), Manganese (Mn), Nickel (Ni), Lead (Pb), Zinc (Zn) and Mercury (Hg) consisting of 3202 sampling stations between 1999 and 2006 (Fig. 1) were utilized in the current research.

    View all citing articles on Scopus
    View full text