Long-Term Trends of Nutrients and Phytoplankton in Chesapeake Bay

Springer Science and Business Media LLC - Tập 39 Số 3 - Trang 664-681 - 2016
Harding, L. W.1, Gallegos, C. L.2, Perry, E. S.3, Miller, W. D.4, Adolf, J. E.5, Mallonee, M. E.6, Paerl, H. W.7
1Department of Atmospheric and Oceanic Sciences, University of California, Los Angeles, Los Angeles, USA
2Smithsonian Environmental Research Center, Edgewater, USA
3Huntingtown, USA
4U. S. Naval Research Laboratory, Washington, USA
5Marine Science Program, University of Hawaii at Hilo, Hilo, USA
6United States Environmental Protection Agency Chesapeake Bay Program Office, Interstate Commission on the Potomac River Basin, Annapolis, USA
7Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, USA

Tóm tắt

Climate effects on hydrology impart high variability to water-quality properties, including nutrient loadings, concentrations, and phytoplankton biomass as chlorophyll-a (chl-a), in estuarine and coastal ecosystems. Resolving long-term trends of these properties requires that we distinguish climate effects from secular changes reflecting anthropogenic eutrophication. Here, we test the hypothesis that strong climatic contrasts leading to irregular dry and wet periods contribute significantly to interannual variability of mean annual values of water-quality properties using in situ data for Chesapeake Bay. Climate effects are quantified using annual freshwater discharge from the Susquehanna River together with a synoptic climatology for the Chesapeake Bay region based on predominant sea-level pressure patterns. Time series of water-quality properties are analyzed using historical (1945–1983) and recent (1984–2012) data for the bay adjusted for climate effects on hydrology. Contemporary monitoring by the Chesapeake Bay Program (CBP) provides data for a period since mid-1984 that is significantly impacted by anthropogenic eutrophication, while historical data back to 1945 serve as historical context for a period prior to severe impairments. The generalized additive model (GAM) and the generalized additive mixed model (GAMM) are developed for nutrient loadings and concentrations (total nitrogen—TN, nitrate + nitrate—NO2 + NO3) at the Susquehanna River and water-quality properties in the bay proper, including dissolved nutrients (NO2 + NO3, orthophosphate—PO4), chl-a, diffuse light attenuation coefficient (K D (PAR)), and chl-a/TN. Each statistical model consists of a sum of nonlinear functions to generate flow-adjusted time series and compute long-term trends accounting for climate effects on hydrology. We present results identifying successive periods of (1) eutrophication ca. 1945–1980 characterized by approximately doubled TN and NO2 + NO3 loadings, leading to increased chl-a and associated ecosystem impairments, and (2) modest decreases of TN and NO2 + NO3 loadings from 1981 to 2012, signaling a partial reversal of nutrient over-enrichment. Comparison of our findings with long-term trends of water-quality properties for a variety of estuarine and coastal ecosystems around the world reveals that trends for Chesapeake Bay are weaker than for other systems subject to strenuous management efforts, suggesting that more aggressive actions than those undertaken to date will be required to counter anthropogenic eutrophication of this valuable resource.

Tài liệu tham khảo

citation_journal_title=Geophysical Research Letters; citation_title=Remotely-sensed chl a at the Chesapeake Bay mouth is correlated with annual freshwater flow to Chesapeake Bay; citation_author=JG Acker, LW Harding, G Leptoukh, T Zhu, S Shen; citation_volume=32; citation_issue=L05601; citation_publication_date=2005; citation_pages=2005; citation_id=CR1 citation_journal_title=Estuarine, Coastal and Shelf Science; citation_title=Environmental forcing of phytoplankton floral composition, biomass, and primary productivity in Chesapeake Bay, USA; citation_author=JE Adolf, CL Yeager, WD Miller, ME Mallonee, LW Harding; citation_volume=67; citation_publication_date=2006; citation_pages=108-122; citation_doi=10.1016/j.ecss.2005.11.030; citation_id=CR2 citation_journal_title=Hydrobiologia; citation_title=Eutrophication in coastal marine ecosystems: towards better understanding and management strategies; citation_author=JH Anderson, DJ Conley; citation_volume=629; citation_publication_date=2009; citation_pages=1-4; citation_doi=10.1007/s10750-009-9758-0; citation_id=CR3 Anonymous. 2000. Directive 200/60/EC of the European parliament and of the council of 23 October 2000 establishing a framework for community action in the field of water policy. Official Journal L 327/1. Boicourt, W.C. 1992. Influence of circulation processes on dissolved oxygen in the Chesapeake Bay. In Oxygen dynamics in Chesapeake Bay: a synthesis of research, ed. D. Smith, M. Leffler, G. Mackiernan, 7–53. College Park: University of Maryland Sea Grant. citation_title=Influence of river flow and nutrient loads on selected ecosystem processes: a synthesis of Chesapeake Bay data; citation_inbook_title=Estuarine science, a synthetic approach to research and practice; citation_publication_date=2000; citation_pages=269-298; citation_id=CR6; citation_author=WR Boynton; citation_author=WM Kemp; citation_publisher=Island citation_journal_title=Estuaries; citation_title=Inputs, transformations, and transport of nitrogen and phosphorus in Chesapeake Bay and selected tributaries; citation_author=WR Boynton, JH Garber, R Summers, WM Kemp; citation_volume=18; citation_publication_date=1995; citation_pages=285-314; citation_doi=10.2307/1352640; citation_id=CR7 Bricker, S., B. Longstaff, W. Dennison, A. Jones, K. Boicourt, C. Wicks, and J. Woerner. 2007. Effects of nutrient enrichment in the Nation’s estuaries: a decade of change. NOAA Coastal Ocean Program Decision Analysis Series No. 26. National Centers for Coastal Ocean Science, Silver Spring, Maryland, USA. 328 p. citation_journal_title=Estuaries and Coasts; citation_title=Historical land use, nitrogen, and coastal eutrophication: a paleoecological perspective; citation_author=GS Brush; citation_volume=32; citation_publication_date=2009; citation_pages=18-28; citation_doi=10.1007/s12237-008-9106-z; citation_id=CR9 citation_journal_title=Limnology and Oceanography; citation_title=Coastal eutrophication and trend reversal: a Danish case study; citation_author=J Carstensen, DJ Conley, JH Andersen, G Ærtebjerg; citation_volume=51; citation_publication_date=2006; citation_pages=398-408; citation_doi=10.4319/lo.2006.51.1_part_2.0398; citation_id=CR10 citation_journal_title=Environmental Science and Technology; citation_title=Connecting the dots: responses of coastal ecosystems to changing nutrient concentrations; citation_author=J Carstensen, M Sanchez-Camacho, CM Duarte, D Krause-Jensen, N Marba; citation_volume=45; citation_publication_date=2011; citation_pages=9122-9132; citation_doi=10.1021/es202351y; citation_id=CR11 citation_journal_title=Marine Ecology Progress Series; citation_title=Our evolving conceptual model of the coastal eutrophication problem; citation_author=JE Cloern; citation_volume=210; citation_publication_date=2001; citation_pages=223-253; citation_doi=10.3354/meps210223; citation_id=CR12 citation_journal_title=Estuaries and Coasts; citation_title=Patterns and scales of phytoplankton variability in estuarine–coastal ecosystems; citation_author=J Cloern, A Jassby; citation_volume=33; citation_publication_date=2010; citation_pages=230-241; citation_doi=10.1007/s12237-009-9195-3; citation_id=CR13 citation_journal_title=Estuarine, Coastal and Shelf Science; citation_title=River discharge controls phytoplankton dynamics in the northern San Francisco Bay Estuary; citation_author=JE Cloern, AE Alpine, BE Cole, RLJ Wong, JF Arthur, MD Ball; citation_volume=16; citation_publication_date=1983; citation_pages=415-429; citation_doi=10.1016/0272-7714(83)90103-8; citation_id=CR14 citation_journal_title=Journal of Sea Research; citation_title=Oligotrophication and emergence of picocyanobacteria and a toxic dinoflagellate in Thau lagoon, southern France; citation_author=Y Collos, B Bec, C Jauzein, E Abadie, T Laugier, J Lautier, A Pastoureaud, P Souchu, A Vaquer; citation_volume=61; citation_publication_date=2009; citation_pages=68-75; citation_doi=10.1016/j.seares.2008.05.008; citation_id=CR15 citation_journal_title=Science; citation_title=Controlling eutrophication: nitrogen and phosphorus; citation_author=DJ Conley, HW Paerl, RW Howarth, DF Boesch, SP Seitzinger, KE Havens, C Lancelot, GE Likens; citation_volume=323; citation_publication_date=2009; citation_pages=1014-1015; citation_doi=10.1126/science.1167755; citation_id=CR16 citation_journal_title=Estuaries and Coasts; citation_title=Return to Neverland: shifting baselines affect eutrophication restoration targets; citation_author=CM Duarte, DJ Conley, J Carstensen, M Sanchez-Camacho; citation_volume=32; citation_publication_date=2009; citation_pages=29-36; citation_doi=10.1007/s12237-008-9111-2; citation_id=CR17 citation_journal_title=Estuarine, Coastal and Shelf Science; citation_title=Phytoplankton, nutrients, and turbidity in the Chesapeake, Delaware, and Hudson estuaries; citation_author=TR Fisher, LW Harding, DW Stanley, LG Ward; citation_volume=27; citation_publication_date=1988; citation_pages=61-93; citation_doi=10.1016/0272-7714(88)90032-7; citation_id=CR18 citation_journal_title=Marine Ecology Progress Series; citation_title=Nutrient limitation of phytoplankton in Chesapeake Bay; citation_author=TR Fisher, ER Peele, JW Ammerman, LW Harding; citation_volume=82; citation_publication_date=1992; citation_pages=51-63; citation_doi=10.3354/meps082051; citation_id=CR19 citation_journal_title=Marine Biology; citation_title=Spatial and temporal variation in resource limitation in Chesapeake Bay; citation_author=TR Fisher, AB Gustafson, K Sellner, R Lacouture, LW Haas, R Magnien, R Karrh, B Michael; citation_volume=133; citation_publication_date=1999; citation_pages=763-778; citation_doi=10.1007/s002270050518; citation_id=CR20 Gallegos, C. L., P. J. Werdell, and C. R. McClain. 2011. Long-term changes in light scattering in Chesapeake Bay inferred from Secchi depth, light attenuation, and remote sensing measurements. Journal of Geophysical Research 116: C00H08, doi:10.1029/JC2011007160. citation_journal_title=Bulletin American Meteorological Society; citation_title=Heavy precipitation and high streamflow in the contiguous United States: trends in the twentieth century; citation_author=PY Groisman, RW Knight, TR Karl; citation_volume=82; citation_publication_date=2001; citation_pages=219-246; citation_doi=10.1175/1520-0477(2001)082<0219:HPAHSI>2.3.CO;2; citation_id=CR22 citation_journal_title=Journal of Hydrometeorology; citation_title=Contemporary changes of the hydrological cycle over the contiguous United States: trends derived from in situ observations; citation_author=PY Groisman, RW Knight, TR Karl, DR Easterling, B Sun, JH Lawrimore; citation_volume=5; citation_publication_date=2004; citation_pages=64-85; citation_doi=10.1175/1525-7541(2004)005<0064:CCOTHC>2.0.CO;2; citation_id=CR23 citation_journal_title=Estuaries and Coasts; citation_title=Hypoxia in Chesapeake Bay, 1950–2001: long-term change in relation to nutrient loading and river flow; citation_author=JD Hagy, WR Boynton, CW Wood, KV Wood; citation_volume=27; citation_publication_date=2004; citation_pages=634-658; citation_doi=10.1007/BF02907650; citation_id=CR24 citation_journal_title=Marine Ecology Progress Series; citation_title=Long-term increase of phytoplankton biomass in Chesapeake Bay, 1950–1994; citation_author=LW Harding, ES Perry; citation_volume=157; citation_publication_date=1997; citation_pages=39-52; citation_doi=10.3354/meps157039; citation_id=CR25 citation_journal_title=Estuarine, Coastal and Shelf Science; citation_title=Phytoplankton production in two east coast estuaries: photosynthesis-light functions and patterns of carbon assimilation in Chesapeake and Delaware Bays; citation_author=LW Harding, BW Meeson, TR Fisher; citation_volume=23; citation_publication_date=1986; citation_pages=773-806; citation_doi=10.1016/0272-7714(86)90074-0; citation_id=CR26 citation_journal_title=Estuarine, Coastal and Shelf Science; citation_title=SeaWiFS retrievals of chlorophyll in Chesapeake Bay and the mid-Atlantic bight; citation_author=LW Harding, A Magnuson, ME Mallonee; citation_volume=62; citation_publication_date=2005; citation_pages=75-94; citation_doi=10.1016/j.ecss.2004.08.011; citation_id=CR27 citation_journal_title=Estuaries and Coasts; citation_title=Multiple lines of evidence for numerical chlorophyll (chl-a) criteria in Chesapeake Bay; citation_author=LW Harding, RA Batiuk, TR Fisher, CL Gallegos, TC Malone, WD Miller, MR Mulholland, H Paerl, ES Perry, P Tango; citation_volume=37; citation_publication_date=2014; citation_pages=134-148; citation_doi=10.1007/s12237-013-9656-6; citation_id=CR28 citation_journal_title=Estuarine, Coastal and Shelf Science; citation_title=Climate effects on phytoplankton floral composition in Chesapeake Bay; citation_author=LW Harding, JE Adolf, ME Mallonee, WD Miller, CL Gallegos, ES Perry, JM Johnson, KR Sellner, HW Paerl; citation_publication_date=2015; citation_id=CR29 citation_journal_title=Journal of the American Water Resources Association; citation_title=Weighted regressions on time, discharge, and season (WRTDS), with an application to Chesapeake Bay river inputs; citation_author=RM Hirsch, DL Moyer, SA Archfield; citation_volume=46; citation_publication_date=2010; citation_pages=857-880; citation_doi=10.1111/j.1752-1688.2010.00482.x; citation_id=CR30 citation_journal_title=Ecosystems; citation_title=Climatic control on eutrophication of the Hudson River estuary; citation_author=RW Howarth, D Swaney, TJ Butler, R Marino; citation_volume=3; citation_publication_date=2000; citation_pages=210-215; citation_doi=10.1007/s100210000020; citation_id=CR31 citation_journal_title=Biogeochemistry; citation_title=The influence of climate on average nitrogen export from large watersheds in the Northeastern United States; citation_author=RW Howarth, DP Swaney, EW Boyer, R Marino, N Jaworski, C Goodale; citation_volume=79; citation_publication_date=2006; citation_pages=163-186; citation_doi=10.1007/s10533-006-9010-1; citation_id=CR32 Jassby, A.D., and J.E. Cloern. 2014. wq: some tools for exploring water quality monitoring data. R package version 0.4-1. http://cran.r-project.org/package=wq . citation_journal_title=Marine Ecology Progress Series; citation_title=Eutrophication of Chesapeake Bay: historical trends and ecological interactions; citation_author=WM Kemp, WR Boynton, JE Adolf, DF Boesch, WC Boicourt, G Brush, JC Cornwell, TR Fisher, PM Glibert, JD Hagy, LW Harding, ED Houde, DG Kimmel, WD Miller, RIE Newell, MR Roman, RM Smith, JC Stevenson; citation_volume=303; citation_publication_date=2005; citation_pages=1-29; citation_doi=10.3354/meps303001; citation_id=CR34 citation_journal_title=Estuaries and Coasts; citation_title=Regional scale climate forcing of mesozooplankton dynamics in Chesapeake Bay; citation_author=DG Kimmel, WD Miller, MR Roman; citation_volume=29; citation_publication_date=2006; citation_pages=375-387; citation_doi=10.1007/BF02784987; citation_id=CR35 citation_journal_title=Estuaries and Coasts; citation_title=Estuarine ecosystem response captured using a synoptic climatology for Chesapeake Bay; citation_author=DG Kimmel, WD Miller, LW Harding, ED Houde, MR Roman; citation_volume=32; citation_publication_date=2009; citation_pages=403-409; citation_doi=10.1007/s12237-009-9147-y; citation_id=CR36 Langland, M.J., P.L. Lietman, P.L., and S.A. Hoffman. 1995. Synthesis of nutrient and sediment data for watersheds within the Chesapeake Bay drainage basin. U.S. Geological Survey Water-Resources Investigations Report 95-4233, 121 p. Langland, M., J. Blomquist, D. Moyer, and K. Hyer. 2012. Nutrient and suspended-sediment trends, loads, and yields and development of an indicator of streamwater quality at nontidal sites in the Chesapeake Bay watershed, 1985–2010. U.S. Geological Survey Scientific Investigations Report 2012-5093, 26 p. Malone T.C. 1992. Effects of water column processes on dissolved oxygen: nutrients, phytoplankton and zooplankton. In Oxygen dynamics in Chesapeake Bay: a synthesis of research, ed. D. Smith, M. Leffler, and G. Mackiernan, 61–112. College Park: University of Maryland Sea Grant. citation_journal_title=Marine Ecology Progress Series; citation_title=Influences of river flow on the dynamics of phytoplankton production in a partially stratified estuary; citation_author=TC Malone, LH Crocker, SE Pike, BW Wendler; citation_volume=48; citation_publication_date=1988; citation_pages=235-249; citation_doi=10.3354/meps048235; citation_id=CR40 citation_journal_title=Estuaries; citation_title=Scales of nutrient limited phytoplankton productivity in Chesapeake Bay; citation_author=TC Malone, DJ Conley, TR Fisher, PM Glibert, LW Harding; citation_volume=19; citation_publication_date=1996; citation_pages=371-385; citation_doi=10.2307/1352457; citation_id=CR41 citation_journal_title=Marine Ecology Progress Series; citation_title=Climate forcing of the spring bloom in Chesapeake Bay; citation_author=WD Miller, LW Harding; citation_volume=331; citation_publication_date=2007; citation_pages=11-22; citation_doi=10.3354/meps331011; citation_id=CR42 citation_journal_title=Geophysical Research Letters; citation_title=Hurricane Isabel generated an unusual fall bloom in Chesapeake Bay; citation_author=WD Miller, LW Harding, JE Adolf; citation_volume=33; citation_issue=L06612; citation_publication_date=2006; citation_pages=2006; citation_id=CR43 citation_journal_title=Water Resources Research; citation_title=Predicting spring discharge of the Susquehanna River from a winter synoptic climatology for the eastern United States; citation_author=WD Miller, DG Kimmel, LW Harding; citation_volume=42; citation_issue=W05414; citation_publication_date=2006; citation_pages=2006; citation_id=CR44 Moyer, D.L., RM. Hirsch, and K.E. Hyer. 2012. Comparison of two regression-based approaches for determining nutrient and sediment fluxes and trends in the Chesapeake Bay watershed. U.S. Geological Survey Scientific Investigations Report 2012–5244, 118 p. ( http://pubs.usgs.gov/sir/2012/5244/ ). citation_journal_title=Estuaries and Coasts; citation_title=Recent trends towards oligotrophication of the Northern Adriatic: evidence from chlorophyll a time series; citation_author=P Mozetić, C Solidoro, G Cossarini, G Socal, R Precali, J France, F Bianchi, C Vittor, N Smodlaka, S Fonda Umani; citation_volume=33; citation_publication_date=2010; citation_pages=362-375; citation_doi=10.1007/s12237-009-9191-7; citation_id=CR46 citation_journal_title=Estuaries and Coasts; citation_title=Long-term trends in Chesapeake Bay seasonal hypoxia, stratification, and nutrient loading; citation_author=RR Murphy, WM Kemp, WP Ball; citation_volume=34; citation_publication_date=2011; citation_pages=1293-1309; citation_doi=10.1007/s12237-011-9413-7; citation_id=CR47 citation_journal_title=Estuarine, Coastal and Shelf Science; citation_title=Potential climate-change impacts on Chesapeake Bay; citation_author=RG Najjar, CR Pyke, MB Adams, D Breitburg, C Hershner, M Kemp, R Howarth, MR Mulholland, M Paolisso, D Secor, K Sellner, D Wardrop, R Wood; citation_volume=86; citation_publication_date=2010; citation_pages=1-20; citation_doi=10.1016/j.ecss.2009.09.026; citation_id=CR48 citation_journal_title=Estuaries and Coasts; citation_title=Nutrient and phytoplankton dynamics in Harima-Nada, eastern Seto Inland Sea, Japan during a 35-year period from 1973 to 2007; citation_author=T Nishikawa, Y Hori, S Nagai, K Miyahara, Y Nakamura, K Harada, M Tanda, T Tada; citation_volume=33; citation_publication_date=2010; citation_pages=224-229; citation_doi=10.1007/s12237-009-9198-0; citation_id=CR49 citation_journal_title=Ophelia; citation_title=Coastal marine eutrophication: a definition, social causes, and future concerns; citation_author=SW Nixon; citation_volume=41; citation_publication_date=1995; citation_pages=199-219; citation_doi=10.1080/00785236.1995.10422044; citation_id=CR50 citation_journal_title=Hydrobiologia; citation_title=Eutrophication and the macroscope; citation_author=SW Nixon; citation_volume=629; citation_publication_date=2009; citation_pages=5-19; citation_doi=10.1007/s10750-009-9759-z; citation_id=CR51 citation_journal_title=Proceedings of the National Academy of Sciences; citation_title=Ecosystem impacts of three sequential hurricanes (Dennis, Floyd, and Irene) on the United States’ largest lagoonal estuary, Pamlico Sound, NC; citation_author=HW Paerl, JD Bales, LW Ausley, CP Buzzelli, LB Crowder, LA Eby, JM Fear, M Go, BL Peierls, TL Richardson, JS Ramus; citation_volume=98; citation_publication_date=2001; citation_pages=5655-5660; citation_doi=10.1073/pnas.101097398; citation_id=CR52 citation_journal_title=Environmental Science and Technology; citation_title=Solving problems resulting from solutions: the evolution of a dual nutrient management strategy for the eutrophying Neuse River Estuary, North Carolina, USA; citation_author=HW Paerl, LM Valdes, MF Piehler, ME Lebo; citation_volume=38; citation_publication_date=2004; citation_pages=3068-3073; citation_doi=10.1021/es0352350; citation_id=CR53 citation_journal_title=Limnology and Oceanography; citation_title=Anthropogenic and climatic influences on the eutrophication of large estuarine ecosystems; citation_author=HW Paerl, LM Valdes, BL Peierls, JE Adolf, LW Harding; citation_volume=51; citation_publication_date=2006; citation_pages=448-462; citation_doi=10.4319/lo.2006.51.1_part_2.0448; citation_id=CR54 citation_journal_title=Estuaries and Coasts; citation_title=Ecological response to hurricane events in the Pamlico Sound System, NC and implications for assessment and management in a regime of increased frequency; citation_author=HW Paerl, LM Valdes, AR Joyner, BL Peierls, CP Buzzelli, MF Piehler, SR Riggs, RR Christian, JS Ramus, EJ Clesceri, LA Eby, LW Crowder, RA Luettich; citation_volume=29; citation_publication_date=2006; citation_pages=1033-1045; citation_doi=10.1007/BF02798666; citation_id=CR55 citation_journal_title=Estuaries and Coasts; citation_title=Phytoplankton community indicators of short- and long-term ecological change in the anthropogenically and climatically impacted Neuse River Estuary, North Carolina, USA; citation_author=HW Paerl, KL Rossignol, NS Hall, BL Peierls, MS Wetz; citation_volume=33; citation_publication_date=2010; citation_pages=485-497; citation_doi=10.1007/s12237-009-9137-0; citation_id=CR56 citation_journal_title=Estuaries and Coasts; citation_title=Hydrologic variability and its control of phytoplankton community structure and function in two shallow, coastal, lagoonal ecosystems: the Neuse and New River estuaries, North Carolina, USA; citation_author=HW Paerl, SN Hall, BL Peierls, KL Rossignol, AR Joyner; citation_publication_date=2013; citation_id=CR57 citation_journal_title=Estuaries; citation_title=Water quality and phytoplankton as indicators of hurricane impacts on a large estuarine ecosystem; citation_author=BL Peierls, RR Christian, HW Paerl; citation_volume=26; citation_publication_date=2003; citation_pages=1329-1343; citation_doi=10.1007/BF02803635; citation_id=CR58 citation_journal_title=Estuaries and Coasts; citation_title=Non-monotonic responses of phytoplankton biomass accumulation to hydrologic variability: a comparison of two coastal plain North Carolina estuaries; citation_author=BL Peierls, NS Hall, HW Paerl; citation_volume=35; citation_publication_date=2012; citation_pages=1376-1392; citation_doi=10.1007/s12237-012-9547-2; citation_id=CR59 citation_journal_title=Estuaries and Coasts; citation_title=Long-term variability of nutrients and chlorophyll in the Chesapeake Bay: a retrospective analysis, 1985–2008; citation_author=MB Prasad, MRP Sapiano, CR Anderson, W Long, R Murtugudde; citation_volume=33; citation_publication_date=2010; citation_pages=1128-1143; citation_doi=10.1007/s12237-010-9325-y; citation_id=CR60 citation_journal_title=Estuaries and Coasts; citation_title=Recovery of Danish coastal ecosystems after reductions in nutrient loading: a holistic approach; citation_author=B Riemann, J Carstensen, K Dahl, H Fossing, JW Hansen, HH Jakobsen, AB Josefson, D Krause-Jensen, S Markager, PA Stæhr, K Timmermann, J Windolf, JH Andersen; citation_publication_date=2015; citation_id=CR61 citation_journal_title=Eos, Transactions American Geophysical Union; citation_title=Chesapeake Bay plankton and fish enhanced by Hurricane Isabel; citation_author=MR Roman, WC Boicourt, DG Kimmel, WD Miller, JE Adolf, LW Harding, ED Houde, S Jung, X Zhang; citation_volume=86; citation_publication_date=2005; citation_pages=261-265; citation_doi=10.1029/2005EO280001; citation_id=CR62 Trenberth, K. E., Jones, P. D., Ambenje, P., Bojariu, R., Easterling, D., Klein, T. A., Parker, D., Rahimzadeh, F., Renwick, J. A., Rusticucci, M., Soden, B., and Zhai, P. 2007. Observations: surface and atmospheric climate change. In Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, ed. S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, and H.L. Miller, 235–336. Cambridge and New York: Cambridge University Press. U.S. Environmental Protection Agency. 1987. 1987 Chesapeake Bay agreement. U.S. Environmental Protection Agency, Chesapeake Bay Program Office, Annapolis, Maryland. U.S. Environmental Protection Agency. 2003. Ambient water quality criteria for dissolved oxygen, water clarity and chlorophyll a for Chesapeake Bay and its tidal tributaries. EPA 903-R-03-002. U.S. Environmental Protection Agency, Region 3, Chesapeake Bay Program Office, Annapolis, Maryland, USA. U.S. Environmental Protection Agency. 2010. Chesapeake Bay phase 5.3 community watershed model. EPA 903S10002 - CBP/TRS-303-10. U.S. Environmental Protection Agency, Chesapeake Bay Program Office, Annapolis, Maryland, USA. citation_journal_title=Limnology and Oceanography; citation_title=Long-term temporal and spatial trends in phytoplankton biomass and class-level taxonomic composition in the hydrologically variable Neuse–Pamlico estuarine continuum, North Carolina, U.S.A; citation_author=LM Valdes-Weaver, MF Piehler, JL Pinckney, KE Howe, K Rossignol, HW Paerl; citation_volume=51; citation_publication_date=2006; citation_pages=1410-1420; citation_doi=10.4319/lo.2006.51.3.1410; citation_id=CR67 citation_journal_title=Estuaries and Coasts; citation_title=Estuarine phytoplankton responses to hurricanes and tropical storms with different characteristics; citation_author=MS Wetz, HW Paerl; citation_volume=31; citation_publication_date=2008; citation_pages=419-429; citation_doi=10.1007/s12237-008-9034-y; citation_id=CR68 citation_journal_title=Estuaries and Coasts; citation_title=Long-term trends of water quality and biotic metrics in Chesapeake Bay: 1986 to 2008; citation_author=MW Williams, S Filoso, BJ Longstaff, WC Dennison; citation_volume=33; citation_publication_date=2010; citation_pages=1279-1299; citation_doi=10.1007/s12237-010-9333-y; citation_id=CR69 citation_journal_title=Journal of the American Statistical Association; citation_title=Stable and efficient multiple smoothing parameter estimation for generalized additive models; citation_author=SN Wood; citation_volume=99; citation_publication_date=2004; citation_pages=673-686; citation_doi=10.1198/016214504000000980; citation_id=CR70 citation_title=Generalized additive models (an introduction with R); citation_publication_date=2006; citation_id=CR71; citation_author=SN Wood; citation_publisher=Chapman & Hall/CRC citation_journal_title=Biometrics; citation_title=Low rank scale invariant tensor product smooths for generalized additive mixed models; citation_author=SN Wood; citation_volume=62; citation_publication_date=2006; citation_pages=1025-1036; citation_doi=10.1111/j.1541-0420.2006.00574.x; citation_id=CR72 citation_title=Synoptic climatology in environmental analysis; citation_publication_date=1993; citation_id=CR73; citation_author=B Yarnal; citation_publisher=Belhaven Press citation_journal_title=Limnology and Oceanography; citation_title=Nutrient loading and meteorological conditions explain interannual variability of hypoxia in Chesapeake Bay; citation_author=Y Zhou, D Scavia, AM Michalak; citation_volume=59; citation_publication_date=2014; citation_pages=373-384; citation_doi=10.4319/lo.2014.59.2.0373; citation_id=CR74