Marine Pollution Bulletin xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera Elizabeth A. Nesbitt a,⇑, Ruth A. Martin a, David E. Martin a, Jude Apple b a b
Earth and Space Sciences Department and Burke Museum, University of Washington, Seattle, WA 9195, USA Padilla Bay National Estuarine Research Reserve, Mount Vernon, WA 98273, USA
a r t i c l e
i n f o
Article history: Received 26 November 2014 Revised 1 June 2015 Accepted 3 June 2015 Available online xxxx Keywords: Benthic foraminifera Puget Sound Pollution Dissolved oxygen Increased acidity
a b s t r a c t Foraminiferal assemblages in sediment grab samples were utilized to evaluate the impacts of anthropogenic activities on benthic habitats in Bellingham Bay, Washington State, U.S.A. Seventy-three samples taken in 1987, 1997, 2006 and 2010 yielded 35 species of foraminifera from 28 genera. Assemblage composition and diversity data indicate a marked deterioration between 1987 and 2010, contrary to the published Chemical Index, but analogous to the situation with macrobiota. Correlation of diversity with chemical pollutants and metals did not identify any significant correlations, however, an unrelated but highly relevant study of bottom water dissolved oxygen concentrations and pH in Bellingham Bay suggests eutrophication with accompanying hypoxia and acidification may be part of the cause. Thus, the metrics of contamination alone do not adequately characterize habitat viability, and benthic foraminiferal assemblages provide insight into the health of coastal ecosystems. Published by Elsevier Ltd.
1. Introduction Environmental protection laws have been passed in many countries to prevent ecosystem degradation by anthropogenic pollution. Some of these laws are particularly designed to protect estuarine and coastal marine environments. In the U.S.A., the Clean Water Act requires the U.S. Environmental Protection Agency (EPA), or delegated states, to develop and implement plans for cleaning up estuaries, rivers, lakes and streams that fail to meet water quality standards. Monitoring the health of ecosystems in marine and estuarine environments frequently employs benthic macrofauna surveys that are assessed against a suite of measured chemical and sedimentological parameters for which standardized methods have been established (Long et al., 2006; Ritter et al., 2011). The Washington State Department of Ecology (WDOE) has various programs for monitoring the water column and the sediment/water interface that have employed these types of analyses in Puget Sound. Samples collected under these programs are used in this study, which focuses on Bellingham Bay, northeastern Puget Sound (Fig. 1). We adopt the definition of Puget Sound used by the National Oceanographic and Atmospheric Administration (NOAA) as all the waters and coastlines of the Salish Sea within the U.S.A.
⇑ Corresponding author. E-mail addresses: [email protected] (E.A. Nesbitt), [email protected] (R.A. Martin), [email protected] (J. Apple).
Here we present an independent assessment of the sediment/water interface utilizing benthic foraminiferal assemblages as a proxy for habitat quality. Benthic foraminifera are excellent indicators of environmental status because of their fast turnover rates, high degree of specialization, and the preservation of dead assemblages in the sediment. In studies of bays and estuaries around the world benthic foraminifera have been used as a measure of pollution and a tool for environmental monitoring (e.g. Alve, 1995; Scott et al., 2005; Coccioni et al., 2009; Schönfeld et al., 2010). An initial comprehensive survey of benthic foraminifera across Puget Sound (Martin et al., 2013) showed that regional, spatial and temporal distribution of foraminiferal assemblages had no clear correlation with the physical parameters of the sediment. Recognizing that diverse biotic and abiotic factors are at play in different permutations within different environments, Martin et al. (2013) acknowledged the need for detailed investigation of each sub-environment of Puget Sound, because all embayments show some evidence of being impacted by anthropogenic activities. Seventy-three sediment samples from Bellingham Bay were analyzed for benthic foraminiferal assemblages from collections in 1987, 1997, 2006 and 2010. In this study, data are presented from the foraminifera assemblages collected in the bay and compared with physical and chemical parameters reported by WDOE. This comparison is supplemented by bottom water dissolved oxygen (DO) concentrations collected over the past several years in Bellingham Bay as part of an ongoing investigation of hypoxia
http://dx.doi.org/10.1016/j.marpolbul.2015.06.006 0025-326X/Published by Elsevier Ltd.
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
2
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Fig. 1. Maps of (a) of Puget Sound, northwestern Washington State, U.S.A., and (b) Bellingham Bay.
conducted at the Northwest Indian College and Western Washington University (Apple et al., 2011). Foraminiferal assemblage data from Bellingham Bay indicate a serious deterioration of environmental conditions at the sediment/water interface from 1997 to 2006. The area has a history of industrial activity and receives inputs of suspended sediment and nutrients from the Nooksack River (Inkpen and Embrey, 1998; Czuba et al., 2011). The waters of Bellingham Bay also include accustomed fishing areas used by the Lummi Tribe, and there is evidence that these are also being adversely impacted (Seiber, 2006). In partnership with NOAA, WDOE implemented a sediment quality monitoring program in Puget Sound in 1989 called the Puget Sound Assessment and Monitoring Program. Support from the State has allowed the program to expand over the years and to include elements from the NOAA National Status and Trends, Bioeffects Monitoring Program, and EPA’s Environmental Monitoring and Assessment Program. This effort has evolved into the Puget Sound Ecosystem Monitoring Program (PSEMP; https:// sites.google.com/a/psemp.org/psemp/). This monitoring of the Puget Sound benthos uses a methodological sequence that combines chemical analyses, toxicants and benthic invertebrate assemblage indicators that are, in turn, integrated into the Sediment Quality Triad Index (SQTI) (Chapman et al., 1987; Long and MacDonald, 1998; Dutch et al., 2009). The system has been modified over the years (Long et al., 2012) to ensure a ‘‘multiple lines of evidence’’ approach described by Bay and Weisberg (2010). A recent review of the current system concluded that this SQTI is valid in producing quality-controlled and reliable data (Ranasinghe et al., 2013). In 2003 Bellingham Bay was among more than 650 water-bodies in Washington State that failed water quality standards (Hood, 2003). Comparison of Bellingham Bay SQTI data from 1997, 2006 and 2010 revealed a significant increase in the area defined as clearly and likely impacted, driven by significantly degraded benthic invertebrate assemblages (Weakland et al., 2013). Bellingham Bay has been the center of activity for numerous industries for more than 150 years. Many of these industries, including coal mining and timber, have left a legacy of contamination in both the soil and the water today. Pollutants include petroleum hydrocarbons, polycyclic aromatic hydrocarbons, phthalates,
pentachlorophenol, dioxins and furans, and metals (including arsenic, cadmium, lead, nickel, zinc, mercury, copper). The most impacted sites are located on the northeastern shoreline, called the Inner Bay (Fig. 1b) which contains particularly toxic areas. A detailed implementation plan to clean up Bellingham Bay was developed by WDOE and EPA and adopted in 2001 (Elardo, 2001; Hood, 2003). Since then a number of agencies have produced reports on progress with clean-up efforts in the water and along the shoreline.
2. Geographic setting Puget Sound is a complex estuarine system that includes numerous small embayments with secondary estuaries, deltas, rocky shores and beaches. Puget Sound (U.S.A.) and the Strait of Georgia (Canada) comprise the Salish Sea, a north–south trending inland waterway that connects to the Pacific Ocean via the Strait of Juan de Fuca (Fig. 1). Because of its proximity to the Pacific Ocean and large tidal exchange, bottom water temperatures, salinity and nutrient content of the Salish Sea are driven predominantly by incoming waters of marine origin. Coastal upwelling, which is strongest during summer months, makes an important contribution to the delivery of cold, acidic, oxygen-depleted water into the Salish Sea and accompanying sub-basins (Masson, 2006; Feely et al., 2010). With over 5600 km2 of waterways that support numerous biological, recreational, cultural and economic resources, the Puget Sound itself is an important resource for the State of Washington. A recent survey found that 93.5% of the Puget Sound shoreline has been modified by humans, with most of the unamended waterfront in the more remote San Juan Islands (Simenstad et al., 2011). Bellingham Bay is a semi-enclosed embayment, approximately 10 km in diameter. It is bordered by the city of Bellingham to the east, known as Inner Bellingham Bay, to the north by agricultural lands and to the west by the rural Lummi Indian Reservation (Fig. 1). The bay is shallow with the maximum depth of 31.3 m in the middle. Tides are the primary driving force for circulation, however the presence of multiple islands near the mouth of the bay dissipate the tidal energy (Wang et al., 2010). Circulation models for the bay indicate a 15 days bottom water residence time
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
(Wang and Yang, submitted), although Rubash and Kilanowski (2007) suggest much longer residence times, thus providing a mechanism for oxygen drawdown in the deeper waters of central Bellingham Bay. Fresh water and sediment enter the bay on the north side from the Nooksack River that rises in the Cascade volcanic mountain range. The Nooksack River has a mean annual discharge of 32,000 cfs and is dominated by winter rainfall events and spring snowmelt. The river is the second largest contributor of suspended sediment to Puget Sound waters (i.e. 1.4 106 tons/yr; Czuba et al., 2011). The delta being built by the Nooksack River continues to prograde southward hundreds of meters each year. Coarser grain-sized suspended sediments are deposited in the lower river, such that the accumulated sediment in the bay is largely silt/clay (Roberts, 1974; Long et al., 2003). Indeed, only three of the 75 sediment samples analyzed as part of the present study were dominated by grain-sizes larger than silt. 3. Methods 3.1. Samples and collection methods Seventy-three sediment samples were used for analysis of foraminiferal assemblages in this study the majority (60) was supplied by PSEMP and the remaining 13 by Robert Harman from a 1987 Shoreline Community College (SCC) program (Fig. 2 and Table 1). Details of sampling sites and protocols are described elsewhere (http://www.ecy.wa.gov/programs/eap/psamp/index.htm) and a discussion on origin and evolution of PSEMP from its inception to the present are provided in Dutch et al. (2009). Samples were recovered using a 0.1 m3 double Van Veen grab sampler, taking the top 2–3 cm off the soft bottom sediments. Part of each grab sample was separated for investigating the structure of infaunal invertebrate communities. The remainder was homogenized for analysis of physical and chemical parameters however these analyses did not include measuring pH and dissolved oxygen (DO. A portion of each homogenized sediment sample was placed into a ZiplocÒ bag and refrigerated for later analysis of its microbiota. PSEMP protocol entails recording field measurements for each sample site: water depth, temperature, salinity of the bottom water, sediment size, sample density, texture, color and odor. Collection methods, reporting requirements, and quality control procedures are summarized in Dutch et al. (2009). The chemical analyses on sediment and interstitial water obtained for most of
3
the field sites include concentrations of 140 metal and semi-volatile organic chemical contaminants up to four invertebrate toxicity tests, and the abundance of infaunal macro-invertebrates identified to the lowest taxonomic level. Taken together these comprise the SQTI parameters, (Long et al., 2006; Dutch et al., 2009, Tables 8 and 10). Because the samples provided to us were months or even years old when we received them, Rose Bengal staining was not effective, thus it was not possible to do live/dead ratios for this study. Sediment was wet-sieved using a 63-lm sieve, air-dried, and 300 benthic foraminifera were picked from each sample. Those samples with very low foraminifera/sediment-grain ratio were floated in trichloroethylene. Some localities yielded very few or no foraminifera. Specimens were placed on micropaleontological slides, and sorted into taxa, with the names following current World Registry of Marine Species protocol. All samples were assigned University of Washington Burke Museum (UWBM) locality numbers and retained in the museum collections. The locations of the WDOE sample sites for this study are provided in Fig. 2; University of Washington Burke Museum catalogue numbers (UWBM), sediment grain size, water depth, bottom water salinity and temperature are given in Table 1. For the SCC samples, the methods of collection, and the measurements of associated physical parameters were very different from those of PSEMP, thus only the taxon assemblage data was included directly into the study presented here. These samples do, however, provide a valuable insight into the conditions of Bellingham Bay a decade before the PSEMP collection program began. As part of a separate collaborative study conducted by Northwest Indian College and Western Washington University (Apple et al., 2011), water quality parameters (i.e. dissolved oxygen, temperature, salinity, pH, and turbidity) were collected in summer months 2007 through 2011 using a SeaBird CTD water column profiler at several stations in the bay. Stations used for this study are not directly coincident with PSEMP stations (Supplementary Table 2) although many are in close proximity to WDOE locations. The data are valuable in understanding the environmental setting of Bellingham Bay. 3.2. Statistical analyses Statistical calculations made for each sample included foraminiferal species richness (number of species per sample) and foraminiferal density (number of individuals/gram dry sediment). The Shannon index (H) was used to measure diversity in order to best account for both species richness and evenness in the samples. One-way ANOVA and the post-hoc Tukey–Kramer test were performed on H and species richness to compare diversity between the different sampling years. Means comparisons and regression analyses were conducted on the data for the two diversity indices. Data were tested for normality using the Kolmogorov–Smirnov/Li lliefors Test. Statistical analyses were done using R Studio 0.98.981 IDE running on top of R version 2.15.2 64-bit edition, with associated contributed software packages. 4. Results 4.1. Physical factors at sample sites
Fig. 2. Locations of foraminiferal sample sites in Bellingham Bay.
In general, benthic foraminifera are constrained in their distribution by the physical parameters at the sediment surface, including sediment grain size, food availability, bottom water, salinity, temperature, pH and DO concentrations. Water depth in Bellingham Bay ranges from 3 m close to the prograding Nooksack delta to 31.3 m in the middle of the bay. Bottom water
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
4
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Table 1 Samples used in this study with locations, Burke Museum catalogue numbers, and depth, temperature and salinity of each where available. Year
Sample #
UWBM #
Lat. degrees
Lat. minutes
Long. degrees
Long. minutes
Depth (m)
1987 1987 1987 1987 1987 1987 1987 1987 1987 1987 1987 1987 1987 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010
SCC1 SCC2 SCC4 SCC5 SCC6 SCC7 SCC8 SCC9 SCC10 SCC11 SCC12 SCC14 SCC15 20 21 22 23 24 25 26 27 28 30 31 32 33 35 36 59 60 4 21 35 53 58 85 101 149 165 195 227 277 299 379 507 4 20 21 22 23 24 25 26 27 28 29 30 31 32 33 35 53 59 60 61 163 195 213 227 277 299 507 42,113
B7851 B7852 B7854 B7855 B7856 B7857 B7858 B7859 B7860 B7912 B7913 B7861 B7862 B7832 B7581 B7697 B7698 B7699 B7700 B7582 B7701 B7702 B7703 B7704 B7705 B7833 B7706 B7707 B7710 B7711 B7620 B7714 B7715 B7716 B7716 B7717 B7718 B7719 B7720 B7721 B7722 B7723 B7724 B7834 B7836 B7727 B7646 B7642 B7836 B7757 B7758 B7759 B7728 B7760 B7729 B7761 B7730 B7731 B7732 B7733 B7734 B7645 B7735 B7736 B7737 B7738 B7837 B7739 B7740 B7741 B7742 B7743 B7744
48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00
45.540 44.760 44.384 44.800 45.090 44.760 44.240 42.850 41.630 40.980 41.330 43.770 44.430 44.263 44.583 45.500 45.085 45.168 45.249 44.883 44.830 44.979 43.997 43.616 43.500 43.016 39.618 40.649 44.283 44.099 41.038 42.624 45.202 43.356 43.361 44.649 41.415 42.172 41.427 45.313 45.202 44.154 44.305 45.015 45.020 41.038 44.267 44.583 45.500 45.083 45.167 45.250 44.883 44.833 44.980 44.317 44.000 43.617 43.500 43.017 45.202 43.361 44.283 44.100 44.183 44.451 45.313 43.461 43.544 44.154 44.305 45.019 45.187
122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00
31.220 31.320 33.059 33.960 35.030 36.630 36.210 36.170 35.960 33.740 29.980 30.980 30.550 36.442 36.543 32.417 30.767 30.650 30.799 30.235 30.083 29.413 30.668 30.949 32.715 32.729 32.983 32.216 29.968 29.953 32.293 32.765 32.176 30.918 30.896 34.045 34.054 32.822 31.271 30.310 35.474 32.773 35.482 29.248 30.224 32.292 36.433 36.533 32.417 30.767 30.650 30.800 30.233 30.083 29.410 30.917 30.667 30.950 32.717 32.733 32.177 30.897 29.967 29.950 30.283 30.304 30.309 33.969 35.474 32.773 35.481 30.225 30.976
2.0 11.0 18.0 5.0 1.0 5.0 9.0 21.0 18.0 27.0 5.0 18.0 10.0 9.5 8.0 7.0 7.5 5.5 5.0 7.5 7.0 7.0 16.0 19.0 28.0 30.0 20.0 24.0 8.5 7.0 25.0 31.3 10.8 13.4 13.4 16.0 29.0 31.0 27.0 4.2 24.0 23.0 13.0 7.8 6.4 25.9 8.3 6.4 3.3 6.0 4.9 6.6 6.1 5.1 5.2 14.0 14.0 18.0 29.0 31.0 12.0 12.0 7.5 5.7 11.0 10.0 4.1 29.0 24.0 24.0 13.0 4.8 8.0
Temp. (°C)
Salinity (PSU)
11.0 11.5 13.5 12.0 12.5 13.0 13.0 14.0 14.0 12.5 10.5 11.0
27 27 24 25 26 24 23 23 14 27 28 30 30 28 30 23 20 30 32
11.0 11.0 13.5 13.5 8.3 9.4 10.1 9.7 9.7 9.7 9.4 9.3 9.3 11.9 9.5 9.3 9.7 10.9 11.9 8.7 10.7 11.5 12.8 11.8 12.5 11.9 11.5 12.5 11.4 9.8 9.7 9.7 9.8 9.3 11.0 9.8 12.0 11.1 10.5 12.0 11.9 9.5 9.3 9.5 9.8 11.9 9.4
29 29 32 32 27
27
30 28 27 23 20 23 25 25 21 23 30 27 26 24 26 23 25 21 25 25 21 23 27 25 25 25 23 26
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx Table 2 Foraminiferal taxa found in all samples in this study. Bolivina pacifica Cushman and McCulloch, 1942 Buccella frigida (Cushman, 1922) Buliminella elegantissima (d’Orbigny, 1839) Cibicides fletcheri Galloway and Wissler, 1927 Cibicides refulgens de Montfort, 1808 Cribroelphidium excavatum (Terquem, 1875) Cribroelphidium magellanicum (Herron-Allen and Earland, 1932) Deuterammina rotaliformis (Heron-Allen and Earland, 1911) Eggerella advena (Cushman, 1922) Elphidiella hannai (Cushman and Grant, 1927) Elphidium frigidum Cushman, 1933) Elphidium gunteri Cole, 1931 Favulina melo (d’Orbigny, 1839) Florilus basispinatum (Cushman and Moyer, 1930) Fursenkoina seminuda (Natland, 1938) Glabratella californiana Lankford and Phleger, 1973 Glandulina sp. Globobulimina sp. Haplophragmoides columbiense Cushman, 1925 Haplophragmoides planissima (Cushman, 1927) Lagena striata (d’Orbigney, 1839) Lagenammina arenulata (Skinner, 1961) Lobatula lobatula (Walker and Jacob, 1798) Miliammina fusca Brady, 1870 Nonionella stella Cushman and Moyer, 1930 Procerolagena gracilis (Williamson, 1848) Quinqueloculina angulostriata Cushman and Valentine, 1930 Quinqueloculina vulgaris d’Orbigny, 1826 Reophax nana Rhumbler, 1913 Reophax scorpiurus de Montfort, 1808 Rotaliammina squamiformis Cushman & McCulloch, 1939 Spiroplectammina biformis (Parker and Jones, 1865) Trochammina hadai Uchio, 1962 Trochammina inflata (Montagu, 1808) Trochammina pacifica Cushman, 1925
temperatures range from 7.7 °C to 10 °C in April and from 9.3 °C to 13.5 °C in July. Salinities range from 21 PSU on the eastern side of the embayment to 32 PSU (Table 1). 4.2. Foraminiferal assemblages and diversity Thirty-five species of foraminifera (28 genera) were recovered from samples in Bellingham Bay (Table 2). The taxon assemblages were dominated by four species that comprised 72% of the total
5
number of foraminifera for all four years (Fig. 3a); Elphidiella hannai (32.9%), Cribroelphidium excavatum (26.9%), Eggerella advena (16.4%) and Buccella frigida (12.1%). The remainder of the taxa were generally found in much smaller numbers, and often in only one or two samples. When the assemblages from different areas and years were considered separately, the same four species were dominant, but in different proportions (Fig. 3b–e). The most notable shift in proportions of species within each assemblage was for the agglutinated taxon E. advena which increased from 4.4% in 1987 to 34.2% of the assemblages in 2010. The shift in proportions of E. advena was concentrated in the Inner Bay (Fig. 4), the section of the Bellingham Bay most impacted by industrial and urban pollution and in the deeper central part of the bay (Fig. 4). The results of one-way ANOVA and the post-hoc Tukey–Kramer HSD test for differences between means of H and species richness are summarized in Table 3. Prior to doing the ANOVA, the Kolmo gorov–Smirnov/Lilliefors Test was done to test for normality. This returned no evidence against normality. ANOVA revealed no significant differences in H (F = 0.77, Pr > F = 0.516). For species richness, however, ANOVA revealed significant differences (F = 7.846, Pr > F = 0.000138). The post hoc Tukey test showed that the significant differences occurred between 1987 and 2010 (p = 0.0198083), 1997 and 2006 (p = 0.0075693), and 1997 and 2010 (p = 0.0004026). The remaining years were not significantly different from one another. Comparisons of species diversity measured using H and species richness are summarized graphically in Fig. 5. Both indices show a declining trend in the diversity of foraminiferal assemblages from 1987 to 2010. The decline in H is less pronounced than that in species richness, possibly because H started low, with a range of 0 to 2.73. In addition, H is not influenced by the larger number of barren stations in 2010 (12 out of 28 in 2010 vs. 5 out of 16 in 2006), because H cannot be calculated when the number of specimens is 0. There is, however, a notable change in species richness between 1997 and 2006, from a mean of six species per sample in 1987 and 1997, to three in 2006, and two in 2010. It is clear from the plots in Fig. 5 that variability increased in both indices from 1987 to 2010. For H, the interquartile (Q1 to Q3) range in 1987 was 0.12 with a mean of 1.563. In 2006, the interquartile range was much larger at 1.23, but the mean was 1.29, while in 2010 the interquartile range was 0.668, with a mean of 1.274. In species richness, the mean number of species present in each sample declined from
Fig. 3. Foraminiferal assemblage composition showing dominant species in each sampling year. (a) All years combined; (b) 1987; (c) 1997; (d) 2006; (e) 2010.
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
6
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Fig. 4. Proportions of the pollution-tolerant, agglutinate species Eggerella advena at each station for each study year. Note that the proportion of this species within each assemblage increases in the later years, and the greatest increases are concentrated in the Inner Bay, the most polluted part of Bellingham Bay.
Table 3 ANOVA of H and species richness for all foraminiferal assemblages. Results of ANOVA and Tukey HSD post hoc tests Shannon index One way ANOVA Df Factor (year) 3 Residuals 50 21 observations deleted due to missingness Tukey multiple comparisons of means 95% family-wise confidence level diff 1997–1987 2006–1987 2010–1987 2006–1997 2010–1997 2010–2006
0.07730308 0.27432692 0.19000000 0.35163000 0.26730308 0.08432692
Sum Sq 1.011 21.885
Mean Sq 0.3369 0.4377
F value 0.77
lwr
upr
p adj
0.7036930 0.5157465 0.4996326 0.3838883 0.3590868 0.8744003
0.9876750 0.7928211 0.8836973 0.5856894 0.6704372 0.9919414
Sum Sq 331.2 985.0
Mean Sq 110.40 14.07
F value 7.846
lwr
upr
p adj
4.5049332 0.3630162 0.4475954 0.9136311 1.7779682 2.9101402
0.8949223 0.0902871 0.0198083 0.0075693 0.0004026 0.9936598
0.5490868 1.0644003 0.8796326 1.0871483 0.8936930 0.7057465
Pr(>F) 0.516
Species richness One way ANOVA Df Factor (year) 3 Residuals 70 Tukey multiple comparisons of means % Family-wise confidence level diff 1997–1987 2006–1987 2010–1987 2006–1997 2010–1997 2010–2006
0.9514170 3.4395604 3.7609890 4.3909774 4.7124060 0.3214286
2.602099 7.242137 7.074383 7.868324 7.646844 3.552997
Pr(>F) 0.000138⁄⁄⁄
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
7
Fig. 5. Box and whisker plots of (a) Shannon index (H) and (b) species richness for Bellingham Bay for all sampling years. For H, median and mean dropped slightly each year, but variance and standard deviation (S.D.) increased, with maxima in 2006. For species richness, mean and median were similar in 1987 and 1997, but then dropped noticeably in 2006 and 2010. As in H, variance and S.D. increased in the later two years, also reaching maxima in 2006.
Fig. 6. Shannon Index (H) at each station during each year of the study, showing spatial distribution and general decrease from 1987 to 2010. The highest H in the study was 2.73 at one station in 2006.
6.154 to 2.321 between 1987 and 2010. Most of the decline took place between 1997 and 2006, where the mean dropped from 6.389 to 2.714 species per sample. As with H, the variability, as demonstrated in the interquartile range, was larger in 2006 (5.75) than in any other year. The spatial distributions of changes in H and species richness across the 4 collecting years are shown in Figs. 6 and 7. The changes are most dramatic in the Inner Bay,
following the patters of increase in percentages of E. advena within the assemblages. Correlation of H and species richness with concentrations of six metals (arsenic, cadmium, copper, mercury, lead and zinc) and total polycyclic aromatic hydrocarbons (PAH) are shown in Figs. 8 and 9. In all cases R2 is small, indicating the concentration of each pollutant examined in this study does not fully explain
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
8
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Fig. 7. Species richness at each station during each year of the study, showing spatial distribution and general decrease from 1987 to 2010. The highest species richness was 20 at one station in 1997.
Fig. 8. Correlations of concentrations of metal pollutants and total PAH with Shannon diversity index (H): (a) arsenic; (b) cadmium; (c) copper; (d) mercury; (e) lead; (f) zinc; (g) total PAH. R2 values indicate that the pollutants analyzed did not explain the variability in the data. Values of p indicate no significant correlation between H and each pollutant.
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
9
Fig. 9. Correlations of concentrations of metal pollutants and total PAH with species richness. (a) arsenic; (b) cadmium; (c) copper; (d) mercury; (e) lead; (f) zinc; (g) total PAH. R2 values indicate that the pollutants analyzed did not explain the variability in the data. Values of p indicate no significant correlation between H and each pollutant.
the variability in the data. In addition, none of the p values indicate significance at the 95% or greater confidence level. Substantial numbers of the calcareous foraminifera, from all years, showed signs of test dissolution, (Supplementary Table 1). Indicators of dissolution were pitting, chalkiness on the surface of the test, holes in tests, and parts of test completely gone. Most commonly found were partial test dissolution and pitting of E. hannai, C. excavatum and B. frigida. In 1997, up to 85% of calcareous individuals per sample showed some degree of partial dissolution. In 2006 and 2010, percentages ranged between 0 and 75%.
5. Discussion The foraminiferal assemblage composition in Bellingham Bay is analogous to foraminiferal assemblages in anthropogenically impacted estuaries elsewhere in the United States and globally. The most common species in this area, E. hannai, C. excavatum, E. advena and B. frigidum are also commonly recorded in such diverse locations as Long Island Sound, Halifax Harbor, western France, Japan, New Zealand and Portugal (Thomas et al., 2000; Scott et al., 2005; Debenay et al., 2006; Hayward et al., 2006; Tsujimoto et al., 2008; Dabbous and Scott, 2012; Martin et al., 2013). The diversity of Bellingham Bay is low compared with outer coast and pristine settings (e.g. Thomas et al., 2000; Tsujimoto et al., 2008). Although all species found in Puget Sound also occur on the outer coast of Washington and southern British Columbia where they are minor components of very diverse assemblages, these species have been shown to be tolerant of environmental stressors. For example, species in the Elphidiidae taxon group are regarded as tolerant of pollution and intermittent hypoxia (Carnahan et al., 2009; Koukousiouraa et al., 2011). In particular, C. excavatum can sequester chloroplasts and has been singled out for being euryhaline and tolerant of many pollutants (Thomas et al., 2000; Debenay et al., 2006; Dabbous and Scott, 2012). E. advena is highly pollution-tolerant, feeding on refractory organic materials and found in large numbers in such environments as
waste discharge areas and Pb–Zn smelter areas (Alve, 1995; McGann et al., 2003; Dabbous and Scott, 2012). B. frigida, a detritivore, generally inhabits deeper water than the others and is typically found in fine-grained sediments with large amounts of organic matter (Thomas et al., 2000). In addition, B. frigida shares dominance with E. advena close to Pb–Zn smelter and fertilizer plant outfalls (Alve, 1995). The Ammonia: Elphidium indicator of Sen Gupta et al. (1996) cannot be used here because Ammonia has not been found in Bellingham Bay. The major components of the foraminiferal assemblages and the low species diversity in Bellingham Bay are typical of anthropogenically impacted areas. The differences in proportions of each dominant species at different sites are not of themselves unusual, as populations fluctuate and distributions can be heterogeneous (Martin et al., 2013). On the other hand, the rapid rise to dominance of the highly pollution-tolerant taxon E. advena over a nine-year period is indicative of deteriorating environmental conditions. Significantly, the greatest increase in the proportion of E. advena as well as the largest decreases in the Shannon index and species richness occur in the Inner Bay, which is the part most impacted by anthropogenic influences (Figs. 4, 6 and 7). These results corroborate the findings of Weakland et al. (2013) that reported a dramatic drop in diversity in benthic macroinvertebrate assemblages in Bellingham Bay from 1997 to 2010. This trend is particularly puzzling since environmental mitigation efforts have been on-going since 1989. Comparisons of SQTI for the years 1997, 2006 and 2010 from the same stations utilized in the study presented here showed that in 2010, the Chemistry Index was only 2% degraded, the Toxicity Index was 10% degraded, but that the Benthic Invertebrate Index showed all sample sites were adversely affected. This reduced the SQTI dramatically, and the data reveal a major change between 1997 and 2006. Thus, the foraminiferal assemblages follow the same trend as the macrobiota data, although no 2010 samples were barren of macroinvertebrates. In marginal marine conditions, diversity is expected to be lower than in open ocean environments because environmental conditions are variable and, at times, challenging. The concern, however,
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
10
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
is the decrease in benthic organismal diversity in Bellingham Bay between 1997 and 2010. Negative correlations between foraminiferal diversity and pollutants are present, but not meaningful. In studies done elsewhere, however, significant negative correlations have been observed between foraminiferal diversity and pollutant concentrations, whether pollution is due to metals, wastewater or hydrocarbons (e.g. McGann et al., 2003; Armynot du Châtelet et al., 2004; Eichler et al., 2012; Martins et al., 2013). Some studies have reported zones barren of foraminifera around outfalls for sewage and heavy metals (e.g. Alve, 1995; Ferraro et al., 2006). In Bellingham Bay, however, barren samples are found throughout the bay, including the middle, deepest parts and nearshore right up into harbors. In 2010 the WDOE reported that 96% of the Bellingham Bay study area had low or minimum exposure to pollutants based on their Chemistry Index, while 74% of the area measured non-toxic or low toxicity on their Toxicity Index (Weakland et al., 2013). The findings of the Weakland report, coupled with our observations of deterioration of the microbenthos in Bellingham Bay, indicate that there is a clear disconnect between the Chemistry and Toxicity indexes and the health of the benthic biota. Variability of bottom water dissolved oxygen (DO) concentrations may
provide a possible explanation for this discrepancy between measures of toxicity and biological response. One of the major problems facing benthic ecosystems is critically low, or hypoxic, DO concentrations that drop below the tolerance of benthic organisms (i.e.
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera Elizabeth A. Nesbitt a,⇑, Ruth A. Martin a, David E. Martin a, Jude Apple b a b
Earth and Space Sciences Department and Burke Museum, University of Washington, Seattle, WA 9195, USA Padilla Bay National Estuarine Research Reserve, Mount Vernon, WA 98273, USA
a r t i c l e
i n f o
Article history: Received 26 November 2014 Revised 1 June 2015 Accepted 3 June 2015 Available online xxxx Keywords: Benthic foraminifera Puget Sound Pollution Dissolved oxygen Increased acidity
a b s t r a c t Foraminiferal assemblages in sediment grab samples were utilized to evaluate the impacts of anthropogenic activities on benthic habitats in Bellingham Bay, Washington State, U.S.A. Seventy-three samples taken in 1987, 1997, 2006 and 2010 yielded 35 species of foraminifera from 28 genera. Assemblage composition and diversity data indicate a marked deterioration between 1987 and 2010, contrary to the published Chemical Index, but analogous to the situation with macrobiota. Correlation of diversity with chemical pollutants and metals did not identify any significant correlations, however, an unrelated but highly relevant study of bottom water dissolved oxygen concentrations and pH in Bellingham Bay suggests eutrophication with accompanying hypoxia and acidification may be part of the cause. Thus, the metrics of contamination alone do not adequately characterize habitat viability, and benthic foraminiferal assemblages provide insight into the health of coastal ecosystems. Published by Elsevier Ltd.
1. Introduction Environmental protection laws have been passed in many countries to prevent ecosystem degradation by anthropogenic pollution. Some of these laws are particularly designed to protect estuarine and coastal marine environments. In the U.S.A., the Clean Water Act requires the U.S. Environmental Protection Agency (EPA), or delegated states, to develop and implement plans for cleaning up estuaries, rivers, lakes and streams that fail to meet water quality standards. Monitoring the health of ecosystems in marine and estuarine environments frequently employs benthic macrofauna surveys that are assessed against a suite of measured chemical and sedimentological parameters for which standardized methods have been established (Long et al., 2006; Ritter et al., 2011). The Washington State Department of Ecology (WDOE) has various programs for monitoring the water column and the sediment/water interface that have employed these types of analyses in Puget Sound. Samples collected under these programs are used in this study, which focuses on Bellingham Bay, northeastern Puget Sound (Fig. 1). We adopt the definition of Puget Sound used by the National Oceanographic and Atmospheric Administration (NOAA) as all the waters and coastlines of the Salish Sea within the U.S.A.
⇑ Corresponding author. E-mail addresses: [email protected] (E.A. Nesbitt), [email protected] (R.A. Martin), [email protected] (J. Apple).
Here we present an independent assessment of the sediment/water interface utilizing benthic foraminiferal assemblages as a proxy for habitat quality. Benthic foraminifera are excellent indicators of environmental status because of their fast turnover rates, high degree of specialization, and the preservation of dead assemblages in the sediment. In studies of bays and estuaries around the world benthic foraminifera have been used as a measure of pollution and a tool for environmental monitoring (e.g. Alve, 1995; Scott et al., 2005; Coccioni et al., 2009; Schönfeld et al., 2010). An initial comprehensive survey of benthic foraminifera across Puget Sound (Martin et al., 2013) showed that regional, spatial and temporal distribution of foraminiferal assemblages had no clear correlation with the physical parameters of the sediment. Recognizing that diverse biotic and abiotic factors are at play in different permutations within different environments, Martin et al. (2013) acknowledged the need for detailed investigation of each sub-environment of Puget Sound, because all embayments show some evidence of being impacted by anthropogenic activities. Seventy-three sediment samples from Bellingham Bay were analyzed for benthic foraminiferal assemblages from collections in 1987, 1997, 2006 and 2010. In this study, data are presented from the foraminifera assemblages collected in the bay and compared with physical and chemical parameters reported by WDOE. This comparison is supplemented by bottom water dissolved oxygen (DO) concentrations collected over the past several years in Bellingham Bay as part of an ongoing investigation of hypoxia
http://dx.doi.org/10.1016/j.marpolbul.2015.06.006 0025-326X/Published by Elsevier Ltd.
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
2
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Fig. 1. Maps of (a) of Puget Sound, northwestern Washington State, U.S.A., and (b) Bellingham Bay.
conducted at the Northwest Indian College and Western Washington University (Apple et al., 2011). Foraminiferal assemblage data from Bellingham Bay indicate a serious deterioration of environmental conditions at the sediment/water interface from 1997 to 2006. The area has a history of industrial activity and receives inputs of suspended sediment and nutrients from the Nooksack River (Inkpen and Embrey, 1998; Czuba et al., 2011). The waters of Bellingham Bay also include accustomed fishing areas used by the Lummi Tribe, and there is evidence that these are also being adversely impacted (Seiber, 2006). In partnership with NOAA, WDOE implemented a sediment quality monitoring program in Puget Sound in 1989 called the Puget Sound Assessment and Monitoring Program. Support from the State has allowed the program to expand over the years and to include elements from the NOAA National Status and Trends, Bioeffects Monitoring Program, and EPA’s Environmental Monitoring and Assessment Program. This effort has evolved into the Puget Sound Ecosystem Monitoring Program (PSEMP; https:// sites.google.com/a/psemp.org/psemp/). This monitoring of the Puget Sound benthos uses a methodological sequence that combines chemical analyses, toxicants and benthic invertebrate assemblage indicators that are, in turn, integrated into the Sediment Quality Triad Index (SQTI) (Chapman et al., 1987; Long and MacDonald, 1998; Dutch et al., 2009). The system has been modified over the years (Long et al., 2012) to ensure a ‘‘multiple lines of evidence’’ approach described by Bay and Weisberg (2010). A recent review of the current system concluded that this SQTI is valid in producing quality-controlled and reliable data (Ranasinghe et al., 2013). In 2003 Bellingham Bay was among more than 650 water-bodies in Washington State that failed water quality standards (Hood, 2003). Comparison of Bellingham Bay SQTI data from 1997, 2006 and 2010 revealed a significant increase in the area defined as clearly and likely impacted, driven by significantly degraded benthic invertebrate assemblages (Weakland et al., 2013). Bellingham Bay has been the center of activity for numerous industries for more than 150 years. Many of these industries, including coal mining and timber, have left a legacy of contamination in both the soil and the water today. Pollutants include petroleum hydrocarbons, polycyclic aromatic hydrocarbons, phthalates,
pentachlorophenol, dioxins and furans, and metals (including arsenic, cadmium, lead, nickel, zinc, mercury, copper). The most impacted sites are located on the northeastern shoreline, called the Inner Bay (Fig. 1b) which contains particularly toxic areas. A detailed implementation plan to clean up Bellingham Bay was developed by WDOE and EPA and adopted in 2001 (Elardo, 2001; Hood, 2003). Since then a number of agencies have produced reports on progress with clean-up efforts in the water and along the shoreline.
2. Geographic setting Puget Sound is a complex estuarine system that includes numerous small embayments with secondary estuaries, deltas, rocky shores and beaches. Puget Sound (U.S.A.) and the Strait of Georgia (Canada) comprise the Salish Sea, a north–south trending inland waterway that connects to the Pacific Ocean via the Strait of Juan de Fuca (Fig. 1). Because of its proximity to the Pacific Ocean and large tidal exchange, bottom water temperatures, salinity and nutrient content of the Salish Sea are driven predominantly by incoming waters of marine origin. Coastal upwelling, which is strongest during summer months, makes an important contribution to the delivery of cold, acidic, oxygen-depleted water into the Salish Sea and accompanying sub-basins (Masson, 2006; Feely et al., 2010). With over 5600 km2 of waterways that support numerous biological, recreational, cultural and economic resources, the Puget Sound itself is an important resource for the State of Washington. A recent survey found that 93.5% of the Puget Sound shoreline has been modified by humans, with most of the unamended waterfront in the more remote San Juan Islands (Simenstad et al., 2011). Bellingham Bay is a semi-enclosed embayment, approximately 10 km in diameter. It is bordered by the city of Bellingham to the east, known as Inner Bellingham Bay, to the north by agricultural lands and to the west by the rural Lummi Indian Reservation (Fig. 1). The bay is shallow with the maximum depth of 31.3 m in the middle. Tides are the primary driving force for circulation, however the presence of multiple islands near the mouth of the bay dissipate the tidal energy (Wang et al., 2010). Circulation models for the bay indicate a 15 days bottom water residence time
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
(Wang and Yang, submitted), although Rubash and Kilanowski (2007) suggest much longer residence times, thus providing a mechanism for oxygen drawdown in the deeper waters of central Bellingham Bay. Fresh water and sediment enter the bay on the north side from the Nooksack River that rises in the Cascade volcanic mountain range. The Nooksack River has a mean annual discharge of 32,000 cfs and is dominated by winter rainfall events and spring snowmelt. The river is the second largest contributor of suspended sediment to Puget Sound waters (i.e. 1.4 106 tons/yr; Czuba et al., 2011). The delta being built by the Nooksack River continues to prograde southward hundreds of meters each year. Coarser grain-sized suspended sediments are deposited in the lower river, such that the accumulated sediment in the bay is largely silt/clay (Roberts, 1974; Long et al., 2003). Indeed, only three of the 75 sediment samples analyzed as part of the present study were dominated by grain-sizes larger than silt. 3. Methods 3.1. Samples and collection methods Seventy-three sediment samples were used for analysis of foraminiferal assemblages in this study the majority (60) was supplied by PSEMP and the remaining 13 by Robert Harman from a 1987 Shoreline Community College (SCC) program (Fig. 2 and Table 1). Details of sampling sites and protocols are described elsewhere (http://www.ecy.wa.gov/programs/eap/psamp/index.htm) and a discussion on origin and evolution of PSEMP from its inception to the present are provided in Dutch et al. (2009). Samples were recovered using a 0.1 m3 double Van Veen grab sampler, taking the top 2–3 cm off the soft bottom sediments. Part of each grab sample was separated for investigating the structure of infaunal invertebrate communities. The remainder was homogenized for analysis of physical and chemical parameters however these analyses did not include measuring pH and dissolved oxygen (DO. A portion of each homogenized sediment sample was placed into a ZiplocÒ bag and refrigerated for later analysis of its microbiota. PSEMP protocol entails recording field measurements for each sample site: water depth, temperature, salinity of the bottom water, sediment size, sample density, texture, color and odor. Collection methods, reporting requirements, and quality control procedures are summarized in Dutch et al. (2009). The chemical analyses on sediment and interstitial water obtained for most of
3
the field sites include concentrations of 140 metal and semi-volatile organic chemical contaminants up to four invertebrate toxicity tests, and the abundance of infaunal macro-invertebrates identified to the lowest taxonomic level. Taken together these comprise the SQTI parameters, (Long et al., 2006; Dutch et al., 2009, Tables 8 and 10). Because the samples provided to us were months or even years old when we received them, Rose Bengal staining was not effective, thus it was not possible to do live/dead ratios for this study. Sediment was wet-sieved using a 63-lm sieve, air-dried, and 300 benthic foraminifera were picked from each sample. Those samples with very low foraminifera/sediment-grain ratio were floated in trichloroethylene. Some localities yielded very few or no foraminifera. Specimens were placed on micropaleontological slides, and sorted into taxa, with the names following current World Registry of Marine Species protocol. All samples were assigned University of Washington Burke Museum (UWBM) locality numbers and retained in the museum collections. The locations of the WDOE sample sites for this study are provided in Fig. 2; University of Washington Burke Museum catalogue numbers (UWBM), sediment grain size, water depth, bottom water salinity and temperature are given in Table 1. For the SCC samples, the methods of collection, and the measurements of associated physical parameters were very different from those of PSEMP, thus only the taxon assemblage data was included directly into the study presented here. These samples do, however, provide a valuable insight into the conditions of Bellingham Bay a decade before the PSEMP collection program began. As part of a separate collaborative study conducted by Northwest Indian College and Western Washington University (Apple et al., 2011), water quality parameters (i.e. dissolved oxygen, temperature, salinity, pH, and turbidity) were collected in summer months 2007 through 2011 using a SeaBird CTD water column profiler at several stations in the bay. Stations used for this study are not directly coincident with PSEMP stations (Supplementary Table 2) although many are in close proximity to WDOE locations. The data are valuable in understanding the environmental setting of Bellingham Bay. 3.2. Statistical analyses Statistical calculations made for each sample included foraminiferal species richness (number of species per sample) and foraminiferal density (number of individuals/gram dry sediment). The Shannon index (H) was used to measure diversity in order to best account for both species richness and evenness in the samples. One-way ANOVA and the post-hoc Tukey–Kramer test were performed on H and species richness to compare diversity between the different sampling years. Means comparisons and regression analyses were conducted on the data for the two diversity indices. Data were tested for normality using the Kolmogorov–Smirnov/Li lliefors Test. Statistical analyses were done using R Studio 0.98.981 IDE running on top of R version 2.15.2 64-bit edition, with associated contributed software packages. 4. Results 4.1. Physical factors at sample sites
Fig. 2. Locations of foraminiferal sample sites in Bellingham Bay.
In general, benthic foraminifera are constrained in their distribution by the physical parameters at the sediment surface, including sediment grain size, food availability, bottom water, salinity, temperature, pH and DO concentrations. Water depth in Bellingham Bay ranges from 3 m close to the prograding Nooksack delta to 31.3 m in the middle of the bay. Bottom water
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
4
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Table 1 Samples used in this study with locations, Burke Museum catalogue numbers, and depth, temperature and salinity of each where available. Year
Sample #
UWBM #
Lat. degrees
Lat. minutes
Long. degrees
Long. minutes
Depth (m)
1987 1987 1987 1987 1987 1987 1987 1987 1987 1987 1987 1987 1987 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 1997 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2006 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010
SCC1 SCC2 SCC4 SCC5 SCC6 SCC7 SCC8 SCC9 SCC10 SCC11 SCC12 SCC14 SCC15 20 21 22 23 24 25 26 27 28 30 31 32 33 35 36 59 60 4 21 35 53 58 85 101 149 165 195 227 277 299 379 507 4 20 21 22 23 24 25 26 27 28 29 30 31 32 33 35 53 59 60 61 163 195 213 227 277 299 507 42,113
B7851 B7852 B7854 B7855 B7856 B7857 B7858 B7859 B7860 B7912 B7913 B7861 B7862 B7832 B7581 B7697 B7698 B7699 B7700 B7582 B7701 B7702 B7703 B7704 B7705 B7833 B7706 B7707 B7710 B7711 B7620 B7714 B7715 B7716 B7716 B7717 B7718 B7719 B7720 B7721 B7722 B7723 B7724 B7834 B7836 B7727 B7646 B7642 B7836 B7757 B7758 B7759 B7728 B7760 B7729 B7761 B7730 B7731 B7732 B7733 B7734 B7645 B7735 B7736 B7737 B7738 B7837 B7739 B7740 B7741 B7742 B7743 B7744
48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00 48.00
45.540 44.760 44.384 44.800 45.090 44.760 44.240 42.850 41.630 40.980 41.330 43.770 44.430 44.263 44.583 45.500 45.085 45.168 45.249 44.883 44.830 44.979 43.997 43.616 43.500 43.016 39.618 40.649 44.283 44.099 41.038 42.624 45.202 43.356 43.361 44.649 41.415 42.172 41.427 45.313 45.202 44.154 44.305 45.015 45.020 41.038 44.267 44.583 45.500 45.083 45.167 45.250 44.883 44.833 44.980 44.317 44.000 43.617 43.500 43.017 45.202 43.361 44.283 44.100 44.183 44.451 45.313 43.461 43.544 44.154 44.305 45.019 45.187
122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00 122.00
31.220 31.320 33.059 33.960 35.030 36.630 36.210 36.170 35.960 33.740 29.980 30.980 30.550 36.442 36.543 32.417 30.767 30.650 30.799 30.235 30.083 29.413 30.668 30.949 32.715 32.729 32.983 32.216 29.968 29.953 32.293 32.765 32.176 30.918 30.896 34.045 34.054 32.822 31.271 30.310 35.474 32.773 35.482 29.248 30.224 32.292 36.433 36.533 32.417 30.767 30.650 30.800 30.233 30.083 29.410 30.917 30.667 30.950 32.717 32.733 32.177 30.897 29.967 29.950 30.283 30.304 30.309 33.969 35.474 32.773 35.481 30.225 30.976
2.0 11.0 18.0 5.0 1.0 5.0 9.0 21.0 18.0 27.0 5.0 18.0 10.0 9.5 8.0 7.0 7.5 5.5 5.0 7.5 7.0 7.0 16.0 19.0 28.0 30.0 20.0 24.0 8.5 7.0 25.0 31.3 10.8 13.4 13.4 16.0 29.0 31.0 27.0 4.2 24.0 23.0 13.0 7.8 6.4 25.9 8.3 6.4 3.3 6.0 4.9 6.6 6.1 5.1 5.2 14.0 14.0 18.0 29.0 31.0 12.0 12.0 7.5 5.7 11.0 10.0 4.1 29.0 24.0 24.0 13.0 4.8 8.0
Temp. (°C)
Salinity (PSU)
11.0 11.5 13.5 12.0 12.5 13.0 13.0 14.0 14.0 12.5 10.5 11.0
27 27 24 25 26 24 23 23 14 27 28 30 30 28 30 23 20 30 32
11.0 11.0 13.5 13.5 8.3 9.4 10.1 9.7 9.7 9.7 9.4 9.3 9.3 11.9 9.5 9.3 9.7 10.9 11.9 8.7 10.7 11.5 12.8 11.8 12.5 11.9 11.5 12.5 11.4 9.8 9.7 9.7 9.8 9.3 11.0 9.8 12.0 11.1 10.5 12.0 11.9 9.5 9.3 9.5 9.8 11.9 9.4
29 29 32 32 27
27
30 28 27 23 20 23 25 25 21 23 30 27 26 24 26 23 25 21 25 25 21 23 27 25 25 25 23 26
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx Table 2 Foraminiferal taxa found in all samples in this study. Bolivina pacifica Cushman and McCulloch, 1942 Buccella frigida (Cushman, 1922) Buliminella elegantissima (d’Orbigny, 1839) Cibicides fletcheri Galloway and Wissler, 1927 Cibicides refulgens de Montfort, 1808 Cribroelphidium excavatum (Terquem, 1875) Cribroelphidium magellanicum (Herron-Allen and Earland, 1932) Deuterammina rotaliformis (Heron-Allen and Earland, 1911) Eggerella advena (Cushman, 1922) Elphidiella hannai (Cushman and Grant, 1927) Elphidium frigidum Cushman, 1933) Elphidium gunteri Cole, 1931 Favulina melo (d’Orbigny, 1839) Florilus basispinatum (Cushman and Moyer, 1930) Fursenkoina seminuda (Natland, 1938) Glabratella californiana Lankford and Phleger, 1973 Glandulina sp. Globobulimina sp. Haplophragmoides columbiense Cushman, 1925 Haplophragmoides planissima (Cushman, 1927) Lagena striata (d’Orbigney, 1839) Lagenammina arenulata (Skinner, 1961) Lobatula lobatula (Walker and Jacob, 1798) Miliammina fusca Brady, 1870 Nonionella stella Cushman and Moyer, 1930 Procerolagena gracilis (Williamson, 1848) Quinqueloculina angulostriata Cushman and Valentine, 1930 Quinqueloculina vulgaris d’Orbigny, 1826 Reophax nana Rhumbler, 1913 Reophax scorpiurus de Montfort, 1808 Rotaliammina squamiformis Cushman & McCulloch, 1939 Spiroplectammina biformis (Parker and Jones, 1865) Trochammina hadai Uchio, 1962 Trochammina inflata (Montagu, 1808) Trochammina pacifica Cushman, 1925
temperatures range from 7.7 °C to 10 °C in April and from 9.3 °C to 13.5 °C in July. Salinities range from 21 PSU on the eastern side of the embayment to 32 PSU (Table 1). 4.2. Foraminiferal assemblages and diversity Thirty-five species of foraminifera (28 genera) were recovered from samples in Bellingham Bay (Table 2). The taxon assemblages were dominated by four species that comprised 72% of the total
5
number of foraminifera for all four years (Fig. 3a); Elphidiella hannai (32.9%), Cribroelphidium excavatum (26.9%), Eggerella advena (16.4%) and Buccella frigida (12.1%). The remainder of the taxa were generally found in much smaller numbers, and often in only one or two samples. When the assemblages from different areas and years were considered separately, the same four species were dominant, but in different proportions (Fig. 3b–e). The most notable shift in proportions of species within each assemblage was for the agglutinated taxon E. advena which increased from 4.4% in 1987 to 34.2% of the assemblages in 2010. The shift in proportions of E. advena was concentrated in the Inner Bay (Fig. 4), the section of the Bellingham Bay most impacted by industrial and urban pollution and in the deeper central part of the bay (Fig. 4). The results of one-way ANOVA and the post-hoc Tukey–Kramer HSD test for differences between means of H and species richness are summarized in Table 3. Prior to doing the ANOVA, the Kolmo gorov–Smirnov/Lilliefors Test was done to test for normality. This returned no evidence against normality. ANOVA revealed no significant differences in H (F = 0.77, Pr > F = 0.516). For species richness, however, ANOVA revealed significant differences (F = 7.846, Pr > F = 0.000138). The post hoc Tukey test showed that the significant differences occurred between 1987 and 2010 (p = 0.0198083), 1997 and 2006 (p = 0.0075693), and 1997 and 2010 (p = 0.0004026). The remaining years were not significantly different from one another. Comparisons of species diversity measured using H and species richness are summarized graphically in Fig. 5. Both indices show a declining trend in the diversity of foraminiferal assemblages from 1987 to 2010. The decline in H is less pronounced than that in species richness, possibly because H started low, with a range of 0 to 2.73. In addition, H is not influenced by the larger number of barren stations in 2010 (12 out of 28 in 2010 vs. 5 out of 16 in 2006), because H cannot be calculated when the number of specimens is 0. There is, however, a notable change in species richness between 1997 and 2006, from a mean of six species per sample in 1987 and 1997, to three in 2006, and two in 2010. It is clear from the plots in Fig. 5 that variability increased in both indices from 1987 to 2010. For H, the interquartile (Q1 to Q3) range in 1987 was 0.12 with a mean of 1.563. In 2006, the interquartile range was much larger at 1.23, but the mean was 1.29, while in 2010 the interquartile range was 0.668, with a mean of 1.274. In species richness, the mean number of species present in each sample declined from
Fig. 3. Foraminiferal assemblage composition showing dominant species in each sampling year. (a) All years combined; (b) 1987; (c) 1997; (d) 2006; (e) 2010.
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
6
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Fig. 4. Proportions of the pollution-tolerant, agglutinate species Eggerella advena at each station for each study year. Note that the proportion of this species within each assemblage increases in the later years, and the greatest increases are concentrated in the Inner Bay, the most polluted part of Bellingham Bay.
Table 3 ANOVA of H and species richness for all foraminiferal assemblages. Results of ANOVA and Tukey HSD post hoc tests Shannon index One way ANOVA Df Factor (year) 3 Residuals 50 21 observations deleted due to missingness Tukey multiple comparisons of means 95% family-wise confidence level diff 1997–1987 2006–1987 2010–1987 2006–1997 2010–1997 2010–2006
0.07730308 0.27432692 0.19000000 0.35163000 0.26730308 0.08432692
Sum Sq 1.011 21.885
Mean Sq 0.3369 0.4377
F value 0.77
lwr
upr
p adj
0.7036930 0.5157465 0.4996326 0.3838883 0.3590868 0.8744003
0.9876750 0.7928211 0.8836973 0.5856894 0.6704372 0.9919414
Sum Sq 331.2 985.0
Mean Sq 110.40 14.07
F value 7.846
lwr
upr
p adj
4.5049332 0.3630162 0.4475954 0.9136311 1.7779682 2.9101402
0.8949223 0.0902871 0.0198083 0.0075693 0.0004026 0.9936598
0.5490868 1.0644003 0.8796326 1.0871483 0.8936930 0.7057465
Pr(>F) 0.516
Species richness One way ANOVA Df Factor (year) 3 Residuals 70 Tukey multiple comparisons of means % Family-wise confidence level diff 1997–1987 2006–1987 2010–1987 2006–1997 2010–1997 2010–2006
0.9514170 3.4395604 3.7609890 4.3909774 4.7124060 0.3214286
2.602099 7.242137 7.074383 7.868324 7.646844 3.552997
Pr(>F) 0.000138⁄⁄⁄
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
7
Fig. 5. Box and whisker plots of (a) Shannon index (H) and (b) species richness for Bellingham Bay for all sampling years. For H, median and mean dropped slightly each year, but variance and standard deviation (S.D.) increased, with maxima in 2006. For species richness, mean and median were similar in 1987 and 1997, but then dropped noticeably in 2006 and 2010. As in H, variance and S.D. increased in the later two years, also reaching maxima in 2006.
Fig. 6. Shannon Index (H) at each station during each year of the study, showing spatial distribution and general decrease from 1987 to 2010. The highest H in the study was 2.73 at one station in 2006.
6.154 to 2.321 between 1987 and 2010. Most of the decline took place between 1997 and 2006, where the mean dropped from 6.389 to 2.714 species per sample. As with H, the variability, as demonstrated in the interquartile range, was larger in 2006 (5.75) than in any other year. The spatial distributions of changes in H and species richness across the 4 collecting years are shown in Figs. 6 and 7. The changes are most dramatic in the Inner Bay,
following the patters of increase in percentages of E. advena within the assemblages. Correlation of H and species richness with concentrations of six metals (arsenic, cadmium, copper, mercury, lead and zinc) and total polycyclic aromatic hydrocarbons (PAH) are shown in Figs. 8 and 9. In all cases R2 is small, indicating the concentration of each pollutant examined in this study does not fully explain
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
8
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
Fig. 7. Species richness at each station during each year of the study, showing spatial distribution and general decrease from 1987 to 2010. The highest species richness was 20 at one station in 1997.
Fig. 8. Correlations of concentrations of metal pollutants and total PAH with Shannon diversity index (H): (a) arsenic; (b) cadmium; (c) copper; (d) mercury; (e) lead; (f) zinc; (g) total PAH. R2 values indicate that the pollutants analyzed did not explain the variability in the data. Values of p indicate no significant correlation between H and each pollutant.
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
9
Fig. 9. Correlations of concentrations of metal pollutants and total PAH with species richness. (a) arsenic; (b) cadmium; (c) copper; (d) mercury; (e) lead; (f) zinc; (g) total PAH. R2 values indicate that the pollutants analyzed did not explain the variability in the data. Values of p indicate no significant correlation between H and each pollutant.
the variability in the data. In addition, none of the p values indicate significance at the 95% or greater confidence level. Substantial numbers of the calcareous foraminifera, from all years, showed signs of test dissolution, (Supplementary Table 1). Indicators of dissolution were pitting, chalkiness on the surface of the test, holes in tests, and parts of test completely gone. Most commonly found were partial test dissolution and pitting of E. hannai, C. excavatum and B. frigida. In 1997, up to 85% of calcareous individuals per sample showed some degree of partial dissolution. In 2006 and 2010, percentages ranged between 0 and 75%.
5. Discussion The foraminiferal assemblage composition in Bellingham Bay is analogous to foraminiferal assemblages in anthropogenically impacted estuaries elsewhere in the United States and globally. The most common species in this area, E. hannai, C. excavatum, E. advena and B. frigidum are also commonly recorded in such diverse locations as Long Island Sound, Halifax Harbor, western France, Japan, New Zealand and Portugal (Thomas et al., 2000; Scott et al., 2005; Debenay et al., 2006; Hayward et al., 2006; Tsujimoto et al., 2008; Dabbous and Scott, 2012; Martin et al., 2013). The diversity of Bellingham Bay is low compared with outer coast and pristine settings (e.g. Thomas et al., 2000; Tsujimoto et al., 2008). Although all species found in Puget Sound also occur on the outer coast of Washington and southern British Columbia where they are minor components of very diverse assemblages, these species have been shown to be tolerant of environmental stressors. For example, species in the Elphidiidae taxon group are regarded as tolerant of pollution and intermittent hypoxia (Carnahan et al., 2009; Koukousiouraa et al., 2011). In particular, C. excavatum can sequester chloroplasts and has been singled out for being euryhaline and tolerant of many pollutants (Thomas et al., 2000; Debenay et al., 2006; Dabbous and Scott, 2012). E. advena is highly pollution-tolerant, feeding on refractory organic materials and found in large numbers in such environments as
waste discharge areas and Pb–Zn smelter areas (Alve, 1995; McGann et al., 2003; Dabbous and Scott, 2012). B. frigida, a detritivore, generally inhabits deeper water than the others and is typically found in fine-grained sediments with large amounts of organic matter (Thomas et al., 2000). In addition, B. frigida shares dominance with E. advena close to Pb–Zn smelter and fertilizer plant outfalls (Alve, 1995). The Ammonia: Elphidium indicator of Sen Gupta et al. (1996) cannot be used here because Ammonia has not been found in Bellingham Bay. The major components of the foraminiferal assemblages and the low species diversity in Bellingham Bay are typical of anthropogenically impacted areas. The differences in proportions of each dominant species at different sites are not of themselves unusual, as populations fluctuate and distributions can be heterogeneous (Martin et al., 2013). On the other hand, the rapid rise to dominance of the highly pollution-tolerant taxon E. advena over a nine-year period is indicative of deteriorating environmental conditions. Significantly, the greatest increase in the proportion of E. advena as well as the largest decreases in the Shannon index and species richness occur in the Inner Bay, which is the part most impacted by anthropogenic influences (Figs. 4, 6 and 7). These results corroborate the findings of Weakland et al. (2013) that reported a dramatic drop in diversity in benthic macroinvertebrate assemblages in Bellingham Bay from 1997 to 2010. This trend is particularly puzzling since environmental mitigation efforts have been on-going since 1989. Comparisons of SQTI for the years 1997, 2006 and 2010 from the same stations utilized in the study presented here showed that in 2010, the Chemistry Index was only 2% degraded, the Toxicity Index was 10% degraded, but that the Benthic Invertebrate Index showed all sample sites were adversely affected. This reduced the SQTI dramatically, and the data reveal a major change between 1997 and 2006. Thus, the foraminiferal assemblages follow the same trend as the macrobiota data, although no 2010 samples were barren of macroinvertebrates. In marginal marine conditions, diversity is expected to be lower than in open ocean environments because environmental conditions are variable and, at times, challenging. The concern, however,
Please cite this article in press as: Nesbitt, E.A., et al. Rapid deterioration of sediment surface habitats in Bellingham Bay, Washington State, as indicated by benthic foraminifera. Mar. Pollut. Bull. (2015), http://dx.doi.org/10.1016/j.marpolbul.2015.06.006
10
E.A. Nesbitt et al. / Marine Pollution Bulletin xxx (2015) xxx–xxx
is the decrease in benthic organismal diversity in Bellingham Bay between 1997 and 2010. Negative correlations between foraminiferal diversity and pollutants are present, but not meaningful. In studies done elsewhere, however, significant negative correlations have been observed between foraminiferal diversity and pollutant concentrations, whether pollution is due to metals, wastewater or hydrocarbons (e.g. McGann et al., 2003; Armynot du Châtelet et al., 2004; Eichler et al., 2012; Martins et al., 2013). Some studies have reported zones barren of foraminifera around outfalls for sewage and heavy metals (e.g. Alve, 1995; Ferraro et al., 2006). In Bellingham Bay, however, barren samples are found throughout the bay, including the middle, deepest parts and nearshore right up into harbors. In 2010 the WDOE reported that 96% of the Bellingham Bay study area had low or minimum exposure to pollutants based on their Chemistry Index, while 74% of the area measured non-toxic or low toxicity on their Toxicity Index (Weakland et al., 2013). The findings of the Weakland report, coupled with our observations of deterioration of the microbenthos in Bellingham Bay, indicate that there is a clear disconnect between the Chemistry and Toxicity indexes and the health of the benthic biota. Variability of bottom water dissolved oxygen (DO) concentrations may
provide a possible explanation for this discrepancy between measures of toxicity and biological response. One of the major problems facing benthic ecosystems is critically low, or hypoxic, DO concentrations that drop below the tolerance of benthic organisms (i.e.
