Eutrophication of Estuarine and Coastal Marine Environments: An Emerging Climatic-Driven Paradigm Shift ()
1. Introduction
Climate change is increasingly hazardous to coastal ecosystems, amplifying the effects of eutrophication and other non-climatic stressors that are causing a decrease in ecosystem services and societal goods and benefits to humankind [1]-[11]. Eutrophication is an insidious degrading process interactive with climatic drivers of change that causes serious escalating problems in estuarine and coastal marine environments traceable to human population growth, land development, and other anthropogenic activities in coastal regions. Of particular note are anthropogenic activities that forge land-use and land-cover changes, modifications of hydrologic regimes, and greater inputs of nutrients and organic matter to coastal waterbodies. These aquatic environments are characterized by highly variable conditions often linked to intense human-mediated alteration of physical, chemical, and biological processes [12]-[19]. Anthropogenic activities on land or in the sea generate endogenic and exogenic pressures (i.e., mechanisms of change) that are agents of ecosystem impacts. A major challenge is to address and effectively manage the cumulative adverse effects of the anthropogenic activities impacting ecosystem structure and function [4] [20]-[22]. Ecosystem-based management and governance are necessary elements to maintain the integrity and sustainability of these vital coastal environments and their services [18] [22]-[26].
This article examines the interaction and impact of climatic drivers of change and eutrophication on estuarine and coastal marine environments. Climate change is defined as regional or global changes in mean climate state or in patterns of climate variability over decades to millions of years often identified using statistical methods, and sometimes referred to as changes in long-term weather conditions [27] [28]. Estuarine and coastal marine ecosystems are changing with escalating climate-induced temperature increases, sea level rise, and nutrient and organic matter loading that are modulating shifts in ecosystem structure and function.
2. Coastal Ecosystem Susceptibility
Estuaries and coastal marine waters are susceptible to the vagaries of natural stressors and the impacts of anthropogenic activities that can create deleterious environmental conditions [1] [6] [8] [14] [15] [29] (Table 1). Numerous physical,
Table 1. Major anthropogenic drivers of change in estuarine and coastal marine environments. Modified from Kennish (100).
Drivers |
Class 1 (Degrade Water Quality) |
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Nutrient Overenrichment and Organic Carbon Loading |
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Thermal Loading |
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Biogeochemical Changes |
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Chemical Contaminants |
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Excessive Sediment/Particulate Inputs |
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Sewage Discharges |
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Pathogens |
Class 2 (Impact Habitat) |
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Watershed Development |
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Land-Use and Land-Cover Changes |
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Marinas and Other Facilities |
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Dredging and Dredged-Material Disposal |
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Mineral Resource Extraction |
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Bottom Trawling |
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Dams and Other Obstructions |
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Shoreline Hardening |
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Lagoon Construction |
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Land Reclamation and Impoundments |
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Coastal Subsidence |
Class 3 (Alter Biotic Communities) |
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Altered Watershed Hydrological Regimes |
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Overfishing |
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Intensive Aquaculture |
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Invasive/Introduced Species |
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Floatables/Plastics/Debris |
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Class 4 (Climate Linked) |
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Climate Change Drivers |
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CO2, CH4, NO2, Chlorofluorocarbons, (Greenhouse Gases) |
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Warming Temperatures |
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Precipitation and Land Runoff |
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Altered Winds and Water Circulation |
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Acidification |
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Extreme Events |
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Heatwaves |
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Hurricanes and Other Major Storms |
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Storm Surges |
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Tornadoes |
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Droughts |
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chemical, and biological factors occur along the freshwater to marine continuum that typically overlap in space and time resulting in cumulative interactive effects, including climatic drivers of change that modulate ecological conditions and impact the structure and function of ecosystems [4] [6] [7] [11] [19] [22]. Increased storm intensity and precipitation, land runoff, river discharges, and warming waters driven by climate change are leading to greater nutrient and organic matter loading, biogeochemical fluxes, harmful algal blooms (HABs), water column stratification and light attenuation, altered circulation, and deteriorated sediment and water quality in estuarine and coastal marine ecosystems [30]-[35]. These factors interacting with other anthropogenic stressors cause significant shifts in organism abundance and productivity, reproduction, phenology, distribution, and food web dynamics. Sea level rise affects water depth, tidal range, salinity, sediment distribution, intertidal and subtidal habitats, and other components of shallow coastal ecosystems. The complexity of the aforementioned interacting factors, the limited databases collected on them, and insufficient use of predictive models generated for specific estuaries and coastal marine waters have created significant challenges for scientists and coastal managers attempting to unravel the array of ecosystem impacts associated with the interactive effects of climatic drivers of change, nutrient enrichment, and organic matter loading in estuarine and coastal marine environments [10].
Multiple and diverse stressors interact additively, synergistically, and antagonistically in estuarine and coastal marine environments [4] [11] [20] [22] [36]. Climatic drivers of change interact with multiple non-climatic anthropogenic stressors to induce pressures in a cumulative way that generate degrading conditions in estuarine and coastal marine environments [37]. For example, the frequency, intensity, and extent of hypoxia are increasing in estuarine and coastal marine waters, where climate change amplifies effects of eutrophication [17] [19] [38]-[41]. Hypoxia and anoxia of bottom waters have devastating impacts on estuarine and marine organisms, often resulting in extensive loss of life in benthic communities and declining fisheries as well as damage to habitats [42]-[44].
It is important, therefore, to assess climatic drivers of change, together with interactive anthropogenic non-climatic stressors such as eutrophication, to delineate and accurately assess the impacts on coastal environments, most notably those affecting physical-chemical conditions and the structure and function of biotic communities. Coastal scientists face significant challenges with such highly variable, interactive, persistent, and damaging drivers of change. This paper focuses on one of these challenges, that is, the effects of climatic drivers of change on eutrophication of estuarine and coastal marine environments, which are causing marked changes in ecosystem condition and sustainability.
3. Coastal Climatic Forcings
Anthropogenic climatic forcings, primarily those factors linked to an inability to curb greenhouse gas emissions (notably carbon dioxide, nitrous oxides, and methane), as well as deforestation and watershed land-use and land-cover changes have increased air and water temperatures and altered biogeochemical cycling and other coastal processes [19] [29] [45]-[47]. As noted previously, climatic forcings have profound effects on freshwater inflow to coastal waterbodies, water column stratification, circulation and mixing, and the distribution of organisms. Modified coastal landscapes and hydrologic systems (e.g., freshwater diversions, river channelization, and dredging) have facilitated nutrient and organic matter loading from point and nonpoint sources into estuarine and coastal marine waters, promoting eutrophication and hypoxia formation and leading to altered ecosystem structure and function [10] [17] [18] [40]. The Sixth Assessment Report of the Intergovernmental Panel on Climate Change (IPCC) documented regional and global impacts of climate change on natural and human systems, including increasingly irreversible biotic and habitat losses in estuarine and coastal marine waters and reduced services they provide [48]. These impacts have been linked directly to greater greenhouse gas emissions (notably CO2), higher global temperatures, sea level rise, increasing nutrient inputs, and decreasing ocean pH levels (acidification). According to Wong et al. (49), coastal ocean acidification driven by climate change is greater in areas affected by eutrophication.
The 2015 Paris Climate Agreement, an international accord on climate change signed by 195 countries, set a long-term goal to limit the increase of global average temperature on Earth to well below 2˚C above pre-industrial levels and to pursue efforts to limit the temperature increase to 1.5˚C above pre-industrial levels. Limiting the global average temperature increase as stated by the Paris Climate Agreement should substantially reduce the environmental risks and effects of climate change on coastal, estuarine, and marine organisms and habitats. Coastal ecosystems are increasingly challenged by major anthropogenic stressors, such as climate change and eutrophication, that require greater focus of management programs to maintain their viability and sustainability [18] [22] [24]-[26]. As global temperature, nutrient enrichment, and organic matter supply continue to increase in many coastal regions, there are greater costs incurred for mitigation, adaptation, and resilience programs needed to deal with their adverse effects, especially in urbanized areas. These programs are necessary to ensure the health of coastal ecosystems and the effectiveness of remediation efforts to prevent their transformation in the face of climate change and other anthropogenic stressors [5] [6] [16] [26].
The record-breaking temperatures on Earth during the past decade have generated a new immediacy to the global existential threat of climate change. Greenhouse gas emissions, largely responsible for increasing global temperatures, reached a record high in 2024, which was also the warmest year on record by far since global temperature records began in 1850, according to the NOAA National Centers for Environmental Information (NCEI). According to the European Union’s Copernicus Climate Change Service (C3C), this was the first ever 12-month period in which the global average surface air temperature increase exceeded the 1.5˚C temperature threshold above the pre-industrial level, reaching 1.6˚C for the year (Figure 1). As conveyed by the C3C, high sea surface temperatures were a significant driver of the elevated annual air temperature anomaly registered for 2024 (Table 2, Figure 2). While 2024 was the warmest year on record (global average surface air temperature 15.10˚C) dating back to 1850, the global average surface air temperature in 2023 was also high (14.98˚C), resulting in a two-year average temperature anomaly for 2023-2024 that exceeded the 1.5˚C temperature threshold as well. Furthermore, the past decade has been the warmest 10-year period in the 175-year climate record of NOAA (NCEI).
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Figure 1. Global surface air temperature increase (˚C) above the average for the pre-industrial reference period (1850-1900) for each month from January 1940 to December 2024, plotted as time series for each year. 2024 is shown as a thick red line and 2023 as a thick pink line, while other years are shown with thin lines and shaded according to the decade, from blue (1940s) to red (2020s). Credit: Copernicus Climate Change Service (C3S)/European Centre for Medium-Range Weather Forecasts (ECMWF). Global Climate Highlights 2024. Source: https://climate.copernicus.eu/copernicus-2024-first-year-exceed-15degc-above-pre-industrial-level.
Table 2. Key temperature statistics of the European Union’s Copernicus Climate Change Service for 2024.
Region |
Anomaly (vs. 1991-2020) |
Actual Temperature |
Rank (out of last 85 years) |
Globe |
+0.72˚C (+1.60˚C vs pre-industrial) |
15.10˚C |
1st |
Europe |
+1.47˚C |
10.69˚C |
1st |
Arctic |
+1.34˚C |
−11.37˚C |
4th highest |
Extra-Polar Ocean |
+0.51˚C |
20.87˚C |
1st |
Credit: Copernicus Climate Change Service (C3S)/European Centre for Medium-Range Weather Forecasts (ECMWF). Global Climate Highlights 2024.
Figure 2. Surface air temperature anomalies on Earth for 2024 relative to the average for the 1991-2020 reference period. Data: ERA5. Credit: Copernicus Climate Change Service (C3S)/European Centre for Medium-Range Weather Forecasts (ECMWF). Global Climate Highlights 2024. Source: https://climate.copernicus.eu/copernicus-2024-first-year-exceed-15degc-above-pre-industrial-level.
The oceans are a major carbon sink and a significant driver of rising global temperatures. The bulk of the aforementioned temperature rise has been borne by the same oceans that absorb ~30% of CO2 emissions; sea surface temperatures have risen as the oceans absorbed ~90% of excess heat stemming from the greenhouse gas emissions. Figure 3 shows sea surface temperature anomalies recorded during 2024. C3C found that the average sea surface temperature (SST) over the extra-polar ocean (between 60˚N - 60˚S) reached a record high of 20.87˚C in 2024. Highest average SST values were recorded in the North Atlantic, Western Pacific, and the Indian Ocean, although most ocean basins had higher than average SST values as well. El Niño Southern Oscillation (ENSO) warming conditions contributed to higher sea temperatures particularly in 2023, while a residual effect extended into the first six months of 2024.
In 2023, the second warmest year on record, the global average land and sea surface temperature was 1.18˚C above the 20th century average of 13.9˚C, as noted by NOAA (NCEI). More than 90% of the warmest years on record have occurred since 2000, reflecting the growing threat of global warming. Since 1850, CO2 concentrations in the atmosphere alone have increased dramatically, mainly due to burning of fossil fuels, rising from approximately 285 parts per million (ppm) to more than 422 ppm at the end of 2024, and likely reaching their highest level in the last 15 million years (NOAA-NCEI). Due to increasing greenhouse gas emissions (mainly CO2), ocean acidification is on the rise as well, threatening corals and other shell-bearing organisms in the sea [45] [46]. To avert the most serious damaging effects of climate change on coastal, estuarine, and marine environments, there is a goal to achieve net-zero CO2 emissions globally by 2050.
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Figure 3. Anomalies and sea surface temperature extremes for 2024. Color categories refer to the percentiles of the temperature distributions for the 1991-2020 reference period. The extreme (“coolest” and “warmest”) categories are based on rankings for the period 1979-2024. Values are calculated only for the ice-free oceans. Data source: ERA5. Credit: Copernicus Climate Change Service (C3S)/European Centre for Medium-Range Weather Forecasts (ECMWF). Global Climate Highlights 2024. Source: https://climate.copernicus.eu/copernicus-2024-first-year-exceed-15degc-above-pre-industrial-level.
The rate of ocean warming has more than doubled since 1993, with most ocean warming occurring since 1980 [49]-[51]. Of great concern are marine heatwaves (i.e., sustained periods of anomalously high near-surface temperatures that can lead to severe and persistent impacts on marine ecosystems), which have doubled in occurrence since the 1980s [52]. They are projected to increase in frequency, duration, and intensity this century with continued climate change [50]. Rising sea temperatures pose an increasing threat to estuarine and coastal marine ecosystems, which rank among the most productive aquatic environments on Earth, providing substantial ecosystem services, goods, and benefits (e.g., recreational and commercial uses, seafood and pharmaceutical products, energy production and coastal protection) for multitudes of people worldwide.
The rate of sea surface temperature increases along coastlines has been greater than that of the open ocean, indicative of the more pressing problems of climate change effects on ecosystems in coastal regions [29] [49]. For example, Lima and Wethy [53] found that over the period from 1982 to 2010 coastal sea surface temperatures increased for more than 71% of the world’s coastlines at a rate of 0.25˚C ± 0.13˚C per decade. In addition to record-breaking temperatures, 2024 exhibited high-intense and destructive tropical and extratropical cyclones as well as other coastal storms accompanied by storm surges that impacted estuarine and coastal marine ecosystems, their watersheds, and nearby built communities. The intensity of major tropical cyclones is increasing due to climate change [8] [9] [19] [49].
The structure and function of estuarine and coastal marine ecosystems are experiencing more intractable changes as temperatures gradually rise and persist above the 1.5˚C temperature threshold noted by the IPCC, including reductions in species abundance, diversity, and fisheries production as well as altered habitats in many regions [45] [46]. Rising temperatures affect the physiological and reproductive processes of estuarine and marine organisms as well as their growth and survival rates [14] [54] [55]. In addition, increasing eutrophication and associated hypoxia/anoxia (hypoxia < 2.0 mg O2 L−1, anoxia < 0.5 mg O2 L−1), influenced in part by rising temperatures together with acidification of susceptible waterbodies, are detrimental to ecosystem function [10] [17]. Furthermore, global warming is promoting the occurrence of toxic, food-web disrupting nuisance and HABs as well as invasive species in coastal ecosystems, which will only worsen with higher temperature increases [19]. The number and expanse of hypoxic zones in estuaries and coastal seas have increased substantially with rising global temperatures and greater eutrophication [17] [39]-[41] [43] [56]-[59]. Dissolved oxygen levels in the sea will decline further with increases in global temperatures this century [50]. Ecosystem services of estuarine and coastal marine ecosystems also will decline with continued global warming, such as fisheries and mariculture, likely leading to food insecurities in some countries as well as diminished tourism and recreational uses in regions worldwide.
Many built communities along coasts are experiencing greater intensity and frequency of extreme weather events and storm surge effects, higher precipitation with nutrient- and organic-enriched river discharges that promote eutrophication, accelerated erosion of beaches and receding shorelines due to sea level rise, and more droughts and heatwaves. Global precipitation over land areas has increased at an average rate of 0.076 cm per decade since 1901 [60]. Climate model forecasts not only predict increased precipitation in the decades ahead but also significant increases in intensity of heavy rainfalls in some regions which will accelerate runoff and freshwater flow into estuaries and coastal marine waters [28]. Other projections reveal regional variations in precipitation, greater storm surges and coastal flooding in areas of heavy precipitation, higher salinity intrusion and coastal erosion, and more coastal community infrastructure damage.
Melting glaciers and ice sheets, as well as thermal expansion of the ocean due to absorption of heat, are accelerating sea level rise, inundation, flooding, increased coastal erosion, salinity intrusion, drowning of wetlands habitat, and loss of coastal infrastructure [46] [49] [61]. Between 1901 and 2018, eustatic mean sea level increased by 20 cm [52], and climate models predict a 40 to >200 cm eustatic sea level rise over the next 100 years [10]. Sea level rise is not globally uniform, but regionally variable, and it therefore poses a greater coastal threat to some regions than others [50].
4. Climatic and Anthropogenic Driver Interactions
Climate change affects nutrient inputs and behavior in estuarine and coastal marine waters by altering temperature, wind, storm occurrence and intensity, hydrologic cycles, water circulation, and sea level rise [2]. Anthropogenic nutrient enrichment and organic matter loading have been increasing in waterbodies along the freshwater to marine continuum since the 1950s, although the interaction of climate change and nutrient enrichment is complex [19] [62]. More data are needed on the effects of multiple anthropogenic factors that interact in a waterbody and alter the structure and function of biotic communities and impact habitats. Medina et al. [63] demonstrated the effectiveness of tracking symptoms of eutrophication over a 22-year period using multiple lines of evidence in a study of the Charlotte Harbor estuary in southwest Florida (USA). Kennish [6] reported that additive, synergistic, and antagonistic interactions of climatic drivers of change and non-climatic anthropogenic stressors are causing significant biotic changes in estuarine and coastal marine waters. Some of the most overt biotic changes are evident in coastal wetlands—salt marshes, mangroves, and seagrasses [5] [64] [65].
Table 3 provides a list of major interactive factors of climate change and non-climatic stressors that contribute to eutrophication development in estuarine and coastal marine environments. An important challenge is determining how climate change forcings interact with nutrient and organic matter loading, freshwater discharges, flushing, and water circulation to alter ecosystems along the freshwater to marine continuum [8] [33] [66]-[68]. Altered frequency, intensity, and timing of precipitation and variable hydrologic conditions linked to climate change are contributing to pulsed nutrient and organic matter delivery as well as modified water column stratification and flushing/residence time in estuaries. These fluxes cause significant changes in nutrient concentrations, primary productivity, and dissolved oxygen levels which influence trophic level dynamics [35] [62] [69]. The flux of hydrologic processes and sea level are affecting biotic communities, habitats, and ecosystem stability [8]. Testa et al. [10] noted that most climate-prediction scenarios of increased global CO2 levels also reflect regional changes in precipitation and storm frequency. For a RCP8.5 “business-as-usual” climate model scenario, Sinha et al. [70] showed that climate-change induced precipitation alone will substantially increase total nitrogen loading in US rivers by 19% ± 14% during this century. In addition, climate change will have a greater effect on dissolved oxygen via altered atmospheric and aquatic forcing effects in coastal environments (i.e., temperature, wind, water column stratification, and water circulation).
Table 3. Major interactive factors of climate change, altered land and hydrologic systems, and eutrophication that exacerbate impacts on estuarine and coastal marine ecosystems.
Factor |
Impact |
Warming Temperatures |
Strengthened Pycnoclines; Reduced Oxygen Transmission to Deeper Waters; Decreased Nutrient Recycling to Surface Waters; Increased Phytoplankton and Vascular Plant Growth and Biomass |
Heatwaves and Droughts |
Decreased Oxygen Solubility |
Coastal Fires |
Increased Runoff of Nutrients and Organic Matter to Coastal Waters from Altered Land Surfaces |
Sea Level Rise |
Coastal Land Inundation and Erosion; Increased Nutrient and Organic Matter Delivery to Estuarine and Coastal Marine Waters |
Storm Surges and Tidal Flooding |
Increased Inundation and Erosion; Runoff of Nutrients and Organic Matter to Streams and Rivers |
Higher Intensity Storms |
Freshwater Runoff Pulses; Higher Nutrient and Organic Matter Delivery to Estuaries and Coastal Marine Waters |
Greater Precipitation
(10% - 20%) |
Increased Land Runoff; Higher Nutrient and Organic Matter Delivery to Estuaries and Coastal Marine Waters |
Land-Use and Land-Cover Changes (Increased Impervious Surfaces) |
Higher Nutrient and Organic Matter Runoff to Streams and Rivers |
Increased Land Runoff |
Higher Nutrient and Organic Matter Delivery to Estuaries and Coastal Marine Waters |
Modified Hydrologic Regimes |
Variable Delivery of Nutrients and Organic Matter Supply to Estuaries and Coastal Marine Waters |
Higher River Discharges |
Greater Nutrient and Organic Matter Loading to Estuarine and Coastal Marine Waters |
Altered Flushing and Water Residence Time |
Variable Concentrations of Nutrients and Organic Matter Supply in Estuarine Waters |
Increased Water Column Stratification |
Reduced Vertical Mixing and Oxygen Delivery to Bottom Waters; Decreased Water Column Nutrient Distributions |
Water Circulation Changes |
Variable Distribution of Nutrients and Organic Matter Supply |
Increased Wind Velocity |
Greater Water Column Mixing and Distribution of Nutrients and Organic Matter |
With ongoing climate change modulation of key processes in estuarine and coastal marine environments, it is vital for management programs to develop the initiatives necessary to mitigate the resulting impacts and improve environmental conditions. To this end, ecosystem-based management using a holistic, multidisciplinary integrated approach that links ecological, physical, and socio-economic systems for the protection and sustainability of these coastal environments is favored [18] [22] [24] [25] [71]-[73]. The entire airshed/watershed to coastal ocean continuum should be addressed by this type of management approach. An example of a relevant nutrient management strategy is that advanced by Paerl et al. [33] for the Neuse River-Pamlico Sound system in North Carolina (USA) that considers holistically the timing of fertilizer applications in coastal watersheds, stormwater controls coupled to climate change, wastewater nutrient releases, no-till agricultural practices, agricultural animal waste containment/treatment, and greater coupling and integration of groundwater and atmospheric nutrient sources with estuarine and coastal nutrient budgets and algal bloom dynamics.
5. Eutrophication
There is an established link between climate change drivers and eutrophication development that poses an increasing threat to biotic communities and habitats in estuarine and coastal marine environments [6]-[8] [17] [19] [40] [62] [74]. Nutrient enrichment and organic matter loading in these environments emerged as an escalating ecological problem during the 1960s and 1970s as human population growth and development accelerated in coastal watersheds worldwide, especially in developed nations [75]-[77]. Approximately 40% of the 8 billion human population on Earth now lives within 100 km of the coast [6]. The impacts of interactive and accelerating climate change drivers and non-climatic anthropogenic stressors are leading to a reexamination of the main factors responsible for declining coastal ecosystems (Table 3).
Eutrophication is defined as an increase in the rate of organic matter supply to an ecosystem [78] [79] and the development of undesirable consequences that pose a threat to its structure (e.g., biotic community composition, species abundance, and biodiversity) and function (e.g., biotic productivity, energy flow, biogeochemical cycling, and microbial decomposition) [7] [32] [80]. It is a hazardous condition manifested by an array of cascading environmental problems such as HABs, hypoxia and anoxia, loss of essential habitat (e.g., seagrass, salt marsh, and shellfish beds), altered biotic communities, reduced biodiversity, species shifts, declining harvestable fisheries, imbalanced trophic food webs, and diminished resilience of impaired waterbodies [6] [19] [81]-[83]. Nutrient and organic matter supply that promotes eutrophication can have an autochthonous source (i.e., via primary and secondary production in the waterbody) as well as an allochthonous source (i.e., transported into the waterbody from terrestrial and other external sources).
Nutrient inputs to a coastal waterbody stimulate phytoplankton and macrophyte primary production and increase autochthonous organic matter inputs, with the biomass accumulation in bottom sediments raising the biochemical oxygen demand and microbial decomposition of the organic matter. Allochthonous inputs of organic matter (e.g., sewage wastes and organism remains originating outside of the waterbody) amplify the effects. Natural coastal hazards, such as landslides, volcanism, and earthquakes, can deliver pulses of organic matter to estuarine and coastal marine environments as well, potentially stressing ecosystems. Nutrient regeneration via microbial decomposition of organic matter in bottom sediments and resuspension processes increase nutrient concentrations in the water column and stimulate additional primary production, which exacerbates nutrient enrichment and eutrophication effects. Burkholder et al. [84] observed that estuarine bottom sediments serve as a secondary source of nutrients for the water column, having concentrations that may be 10- to 100-fold higher than in the water column. Thus, pelagic-benthic coupling plays a significant role in biogeochemical feedbacks that can lead to overenrichment of nutrients in the waterbody exacerbating eutrophication problems [77]. Nutrient overenrichment and organic matter loading problems are frequently observed in waterways near major cities where anthropogenic activities are greatest (e.g., New York City, São Paulo, Tokyo, Cairo, and Stockholm). Eutrophication is a major aquatic pollution problem in the world today, with more than two-thirds of US estuaries alone impacted by it [14] [32] [77].
High inputs of nutrients stimulate phytoplankton and macroalgal blooms, which can increase shading effects, hypoxia, and loss of seagrasses and other phanergams that serve as vital benthic habitats for biotic communities [38] [81] [83]-[86]. Excessively high water temperatures in summer linked to climate-change driven heatwaves can decimate seagrass beds, particularly at species range boundaries where water temperatures approach species thermal tolerance limits, as is evident in Zostera marina beds in Chesapeake Bay and other Mid-Atlantic estuaries [13] [86]. These cascading problems cause disruption of system trophodynamics and declining resilience. Consequently, nutrient controls (i.e., nutrient load reductions) implemented along the freshwater to marine continuum are a key strategy of water-quality management programs to remediate adverse effects of nutrient enrichment and organic matter loading. Allochthonous transport systems that deliver nitrogen and phosphorus to estuaries and coastal marine waters are necessary targets for nutrient reduction efforts (i.e., nutrients in land runoff and river discharges, wastewaters, groundwater, and atmospheric deposition). Nonpoint source nutrient inputs are more difficult to control than point sources because they are widely dispersed and temporally variable. While many investigators emphasize the importance of nutrient inputs from land runoff, river discharges, and wastewater systems, others are contending that groundwater and ocean water sources cannot be ignored in eutrophication assessment as well [87] [88]. For example, Rocha et al. [88] estimated that 14% of the nitrogen and 3.9% of the phosphorus inputs into agroecosystems arrives at sea via groundwater-borne discharges.
Human-altered physical and biological systems can significantly enhance eutrophication. For example, hydromodifications in coastal watersheds can facilitate nutrient-enriched freshwater discharges to estuaries and coastal marine waters and thus can promote higher primary production in receiving waters. In addition, overfishing may lead to the reduction of top-down grazing pressure and potentially greater phytoplankton and macrophyte growth [74].
Allochthonous nitrogen inputs, originating outside of an estuary, are generally referred to as new nitrogen rather than nitrogen generated autochthonously [89]. The effects of climate change are now augmenting non-climatic, anthropogenic-driven nutrient enrichment and organic matter loading, hypoxia development, and resulting biotic impacts, thereby posing even greater challenges for coastal ecosystem management programs that must deal with both global and local drivers of ecosystem change [2] [58] [66] [69] [74] [90] [91]. Management strategies to control nutrient overenrichment of coastal waterbodies must consider the nutrient sources, concentrations, delivery processes, and effects along the entire freshwater to marine continuum, all of which pose significant challenges to coastal resource managers.
Eutrophication affects the trophic status of an estuary, which can be expressed as a trophic state index (TSI) in units of C per area per unit time organized into four categories (i.e., oligotrophic <100 g C m−2·yr−1, mesotrophic 100–300 g C m−2·yr−1, eutrophic 300 - 500 g C m−2·yr−1, and hypereutrophic > 500 g C m−2·yr−1). There are several main factors that must be considered when assessing the TSI and the ecosystem responses to eutrophication, including: 1) nutrient concentrations in the estuary; 2) nutrient sources; 3) export rates (i.e., flushing, microbially-mediated losses through respiration and denitrification); and 4) nutrient recycling/regeneration rates [89]. Management measures needed to mitigate the symptoms and effects of eutrophication should not only focus on nitrogen and phosphorus inputs (primarily inorganic nitrogen and phosphorus as well as organic forms) but also the hydrologic controls of their delivery to an estuary or coastal marine waterbody, and the methods of nutrient reduction to be implemented.
Remediation of environmental impacts in the US typically includes regulations to protect receiving waters and the application of Total Maximum Daily Loads (TMDL) to limit the amount of nutrient inputs to a receiving waterbody. For example, in 2010, the U.S. Environmental Protection Agency (USEPA) set the Total Maximum Daily Load limits on the amount of nitrogen and phosphorus allowed to enter Chesapeake Bay (USA). According to the USEPA [92], a TMDL establishes the maximum amount of a pollutant allowed to enter a waterbody so that the waterbody will meet and continue to meet water quality standards for that particular pollutant. In addition to documenting a pollutant reduction target, it allocates the load reductions necessary to the source(s) of the pollutant to achieve the overall target. A TMDL is considered part of Section 303(d) of the Clean Water Act, which specifies the process for identifying impaired waters and developing plans to restore them.
Eutrophication of estuarine and coastal marine environments increased dramatically after 1970. It remains a serious global environmental concern today as watershed development and poor land-use practices have removed soils and vegetation, creating more impervious land cover that accelerates runoff and delivery of nutrients and organic matter to rivers and streams (Table 3). These anthropogenic changes have contributed to widespread and pervasive water quality problems in estuarine and coastal marine waters [6]-[8] [38] [62] [74] [76]. The threat of coastal eutrophication is continuing to increase with climate change [7] [17] [19] [93]-[95]. The amount of reactive nitrogen and phosphorus entering estuarine and other coastal marine waters has increased dramatically over the past several decades with greater use of agricultural fertilizers and fossil fuels, and escalating climate change causing significant ecosystem impacts [87] [96]-[98].
Climate change is an increasingly important factor in eutrophication development in estuarine and coastal marine environments due in part to the greater interaction between atmospheric forcing factors and availability of nutrients [19] [33]. As inferred above, higher precipitation in many regions increases runoff of nutrients from agricultural lands and fertilized lawns, and they stimulate primary production and organic matter accumulation in receiving waters. It also modulates flushing and water residence times. Pulsed freshwater discharges from storms and land runoff strengthen stratification of coastal waterbodies and restrict exchange of surface and bottom waters, resulting in deoxygenation of deeper waters via microbial-mediated decomposition of organic matter.
Climate models predict heavier regional precipitation intensity (up to ~15% - 20% greater) due to climate change, although the regions of elevated precipitation will vary. Frid and Caswell [55] indicated a possible 50% increase in precipitation above 50˚N latitude and up to a 20% decrease between 20˚ and 50˚N and ˚S latitudes. For some of the locations experiencing heavier precipitation and runoff, nutrient overenrichment and excessive organic matter supply will escalate environmental impacts and potentially decrease ecosystem services and reduce goods and benefits (e.g., fish and shellfish production) for human use [18]. More sediments will reach estuarine and coastal marine waters affecting water column turbidity and the benthic habitat. Flushing rates in estuaries will increase as well, while water residence times will decrease. Variable wind patterns can shift salinity regimes, water circulation, and water column mixing, influencing dissolved oxygen levels in deeper waters and organism distribution. Rising sea levels will increase salinization of estuaries, modulating the species composition of biotic communities upestuary.
Higher water temperatures and salinities strengthen pycnoclines and reduce diffusion of oxygen to bottom waters as well as nutrient recycling to surface waters. Reduced wind velocities in some regions can hinder vertical mixing and reoxygenation of oxygen-depleted bottom waters as well as decrease water column nutrient distributions, thereby affecting primary production and food-web dynamics. With elevated organic matter supply and increased respiratory demand for oxygen below the pycnocline, conditions are favorable for hypoxia formation [40]. Additionally, higher temperatures lower oxygen solubility, increase metabolism and mineralization rates, and lead to greater production of organic matter, compounding water quality problems that affect the abundance and distribution of organisms [14] [18] [74]. With less dissolved oxygen transmission to deeper waters and greater microbial decomposition of organic matter in and on bottom sediments, oxygen-depleted bottom waters can spread hypoxic or anoxic conditions over extensive areas, endangering biotic communities and habitats over broad areas [10] [17] [40] [41] [59]. In addition, declining oxygen concentrations affect biogeochemical cycling of nutrients and other substances that affect phytoplankton production and the trophic balance of an ecosystem [17]. Bottom sediments are a sink for nutrient inputs, while benthic-pelagic coupling represents an important link returning nutrients from bottom sediments to the water column, which can exacerbate eutrophication impacts in estuaries [10]. Hypoxia affects ecosystems extending from shallow estuaries through coastal ocean and open ocean waters to depths of 600 - 700 m [40]. These waters include some of the most productive aquatic ecosystems on Earth.
Seasonal and multi-annual hydrologic variability (wet and dry-drought periods—El Niño and La Niña years), higher intensity hurricane activity, nor-easters, and severe summer thunderstorms interact with non-climatic anthropogenic stressors to impact estuarine and coastal marine ecosystem processes [19] [35] [62] [81]. Stronger winds associated with a warmer planet and more extreme intense storms with heavy rainfall create hydrologic complexity with increased water column mixing, altered water circulation patterns, and changing salinity regimes in coastal waters affecting organism abundance, distribution, and trophodynamics [6]. They affect longshore currents and the upwelling systems that deliver nutrients from offshore ocean waters, contributing to nutrient enrichment of nearshore waters [87]. Upwelling of nutrient-rich deep ocean waters into nearshore areas often stimulate massive phytoplankton blooms that can impact fisheries and aquaculture fish farms.
A major concern is the occurrence of HABs which are on the rise in estuaries and coastal marine waters with increasing climate change [19]. HABs include environmentally damaging taxonomic groups (e.g., cyanobacteria, red-tide dinoflagellates, and brown-tide pelagophytes) that impair water quality and pose a threat to shellfish and biotic communities as well as a potential danger to humans consuming contaminated seafood products [14]. High rainfall by tropical cyclones, such as those commonly striking the North Carolina coast (USA), foster nutrient and organic matter loading, increasing primary production, and mediating eutrophication, leading to significant biogeochemical changes along the freshwater to marine continuum [19] [99]. For example, there have been 38 tropical storms striking North Carolina’s coastal areas over the past three decades, including Hurricanes Floyd (1999), Matthew (2016), and Florence (2018) that delivered unprecedented amounts of rainfall and flooding waters, causing significant biotic changes in the Albemarle-Pamlico estuarine system [19] [95].
Seitzinger et al. [93] noted that nutrient loading effects are not only contingent upon the concentration of nutrients in freshwater discharges but also on the nutrient forms and nutrient ratios that occur. They also observed that anthropogenic loading of dissolved inorganic nutrients (DIN, DIP) to coastal ecosystems is two to three times greater than delivered by natural processes, reflecting the overwhelming influence of human activities on nutrient dynamics and water quality conditions in estuarine and nearshore ocean waters. Coastal areas that have less nutrient management also exhibit the highest nutrient inputs to the coastal zone. Because of the large human coastal population, unmanaged or poorly managed waters in coastal watersheds substantially increase nutrient loading and associated impacts in estuarine and coastal marine waters [100] [101].
Nutrient overenrichment is often most evident in shallow coastal bays, lagoons, and semi-enclosed estuaries with restricted circulation, low flushing rates, and relatively long water residence times that receive nutrients from highly developed coastal watersheds with agricultural activity [19] [83] [102] [103]. Many of these shallow ecosystems are eutrophied with nutrient loading stimulating excessive phytoplankton and benthic macrophyte production leading to elevated autochthonous loads of organic matter and oxygen-depleted bottom waters detrimental to benthic communities with impacts reverberating through upper trophic levels. Hypoxia is often more episodic in the shallower (1 - 5 m) than the deeper coastal waterbodies, fluctuating over time scales of hours to days or even weekly depending on whether the water column is well mixed by wind activity or periodically stratified. In contrast, hypoxia in deeper stratified estuaries and coastal shelf waters (10 - 50 m) can persist over a summer season or longer, such as in Chesapeake Bay and Long Island Sound [10] [40].
In shallow estuaries, eutrophication typically causes a shift in dominance from seagrasses and perennial macroalgae to ephemeral, bloom-forming macroalgae and epiphytes that affect benthic faunal communities [103] [104]. However, eutrophication and hypoxia development in many of these shallow ecosystems are often less well studied than in larger, deeper and more prominent estuarine and coastal marine ecosystems [77]. Bottom habitats typically lie within the photic zone in these shallow ecosystems, which enhances their primary production and promotes eutrophication when nutrient inputs are elevated [13]. Since coastal lagoons occupy about 13% of coastal shorelines worldwide and are highly responsive to nutrient and chemical contaminant inputs, they require the focus of sound and careful management practices for successful environmental and resource sustainability [102].
Coastal wetlands are vulnerable to increasing temperatures, rising sea levels, and nutrient enrichment, and these factors have taken a toll. Rising sea levels are shifting shorelines landward, eroding salt marshes and other coastal wetlands habitat, and endangering their sustainability [65]. Wetlands upland migration in response to sea level rise is obstructed in many areas due to human shoreline defense structures that create coastal squeeze and the loss of wetlands habitat, rendering developed communities in coastal watersheds more vulnerable to storms, flooding, and other hazards. Other direct anthropogenic impacts (e.g., land reclamation and impoundments) have caused destruction of wetlands habitat as well [18].
Gedan et al. [105] and Deegan et al. [106] found that eutrophication is a driver of structural salt marsh community losses in New England (USA). In experimental work on Spartina alterniflora marsh, Deegan et al. [106] showed that at nitrogen levels commonly associated with coastal eutrophication there were significant impacts, including creek-bank collapse and conversion of creek-bank marsh to unvegetated mud, indicating excessive nutrient loading impacted the habitat. Reef et al. [107] indicated that eutrophication also negatively impacts mangroves. In addition, Lotze et al. [15] reported that eutrophication is responsible for increasing fragmentation, depletion, and complete loss of seagrass habitat; Orth et al. [108] (2006) and Waycott et al. [109] emphasized that eutrophication poses a serious threat to seagrass ecosystems globally. About 25% - 50% of coastal wetlands worldwide have been lost over the past 50 years, mainly due to anthropogenic effects [110]. Since they are vital blue carbon habitats for the sequestration of CO2, accounting for the storage of nearly 50% of the total organic carbon buried in marine sediments, their losses have been particularly problematic for mitigating climate change effects in coastal ecosystems.
6. Nutrient Limitation
Nitrogen and phosphorus are the most important limiting nutrients to primary production in aquatic ecosystems [76] [111]. Nitrogen is generally the dominant limiting nutrient in most estuarine and coastal marine environments [35] [76] and is mainly responsible for eutrophication development there [10]. Phosphorus is the primary limiting nutrient in freshwater ecosystems as well as some estuaries, such as Apalachicola Bay on the northwest coast of Florida (USA). In addition, some estuarine and coastal marine ecosystems exhibit nitrogen and phosphorus co-limitation [112]. Both nitrogen and phosphorus are important in many brackish water systems such as in the Baltic region [10]. Furthermore, nitrogen or phosphorus limitation of primary production may change temporally and spatially in the same waterbody, with phosphorus typically limiting in the spring and nitrogen limiting in the summer. Low silica levels can limit primary production of marine diatoms. This phytoplankton group can produce extensive spring blooms in temperate estuaries and coastal marine waters. Nutrient availability is an important factor in whether primary production is either nitrogen or phosphorus limited [87]. Because changes in nutrient limitation commonly occur along the freshwater to marine continuum, reduction of both nitrogen and phosphorus loading should be given high priority by management programs tasked with mitigating HABs and other water quality problems that develop [19] [113]. Nutrient concentrations vary considerably in estuarine ecosystems because of multiple nutrient inputs from terrestrial, marine, and atmospheric sources, as well as the flux of biotic uptake, sedimentation, denitrification, mineralization of organic matter, and nutrient transport to offshore waters [14] [16].
Nitrogen and phosphorus availability differs in estuarine and coastal marine environments. For example, much phosphorus entering these environments is sorbed to sediment and organic particles and thus may not be bioavailable. Greater development of coastal watersheds over the past several decades has increased the bioavailability of reactive nitrogen in estuaries. Galloway et al. [96] recounted that the largest sources of reactive nitrogen are inorganic nitrogen in fertilizers, NOx emissions from fossil-fuel combustion, and nitrogen fixation in agricultural lands. Howarth and Marino [76], Seitzinger et al. [93], Seitzinger and Phillips [94], and Howarth et al. [98] stressed that increased use of reactive nitrogen in fertilizers and greater land runoff have been a significant driver of eutrophication occurrence in coastal ecosystems. Since the onset of greater anthropogenic nutrient loading of rivers and estuaries in the 1950s, 1960s and 1970s, eutrophication impacts have become more pervasive and acute, including declining water quality, altered biogeochemical processes and biotic communities, and the loss of vital habitats (e.g., seagrasses, shellfish beds, and coral reefs) [7] [32] [49] [110]. Howarth et al. [97] stated that chemical fertilizer use increased dramatically after WWII, being a major contributor to eutrophication development in subsequent years in estuarine and coastal marine waters. Diffuse sources of nutrients from agricultural and urban land areas have become more important than point source inputs for eutrophication and hypoxia development in coastal ecosystems [17] [19] [30] [76] [112] [114].
Howarth et al. [98] reported that over nearly a four-decade period (1961 to 1997), the total reactive nitrogen export in rivers to the coastal ocean nearly doubled from 3.0 Tg N yr−1 to 5.0 Tg N yr−1. Climate change has also become an increasingly important driver of nutrient pollution in coastal ecosystems [2] [29]. Many U.S. estuaries are moderately to highly eutrophic today due largely to human-mediated activities linked to greater land-use and land-cover modifications in coastal watersheds [6] [14] [82].
The trophodynamics of estuarine and coastal marine ecosystems have been significantly affected by eutrophication in which primary producers respond to bottom-up physical-chemical drivers (nutrients, light, temperature) and top-down controls (grazers and predators), leading to altered food-web structure that affects fishery yields and other ecosystem services [18] [49] [81]. In these ecosystems, characterized by highly variable hydrology, salinity, nutrients, and other factors, the species composition, abundance, diversity, and distribution of organisms often change considerably both spatially and temporally, with massive kills of fish and benthic invertebrates commonly occurring in deoxygenated bottom waters [39] [57] [58]. Nutrient overenrichment, algal bloom formation, and epiphytic overgrowth of vegetation surfaces reduce or block light transmission to submerged aquatic vegetation (e.g., seagrass beds) and, in extreme cases, result in the total dieback of this critically important benthic habitat [6] [8] [85] [86]. The insidious degrading effects of eutrophication and the deleterious impacts of hypoxia can significantly reduce productive commercial and recreational fisheries and decrease human use of these coastal ecosystems [18] [39] [57] [58] [83].
Howarth and Marino [76] estimated that nitrogen fluxes to the U.S. coast alone increased by a sixfold measure compared to previous decades and reached even higher numbers in the North Sea and other coastal waterbodies. Nutrient overenrichment is a primary causative factor for increased (nuisance and toxic) algal blooms and hypoxia development, which can substantially reduce ecosystem services. As noted previously, HABs are hazardous to estuarine and coastal marine organisms, particularly benthic communities adversely affected by shading effects and deoxygenation in deeper waters. For example, Karenia brevis is a dinoflagellate that forms red tides and produces a potent toxin (brevetorin) causing fish kills. Humans consuming shellfish contaminated with toxins from red tides can develop paralytic shellfish poisoning, a life-threatening illness that damages nervous, respiratory, and cardiovascular systems. Aureococcus anophagefferens, a brown-tide pelagophyte, impairs the growth of shellfish populations (e.g., hard clams, Mercenaria mercenaria), reducing their market value.
The prevailing view of coastal scientists today regarding the optimal management of eutrophication in estuarine and coastal marine environments is the dual reduction of nitrogen and phosphorus loadings [35] [87] [112] [114]-[116]. Watershed management strategies employ multiple corrective measures for controlling eutrophication, including adapting low-impact development and best management practices in watersheds, upgrading stormwater controls, advancing open space preservation, enhancing riparian buffers and wetlands habitat, and implementing government regulatory measures to limit nutrient loading (e.g., Total Maximum Daily Loads –TMDLs) [102]. Seitzinger et al. [93] stressed the need for a holistic integrated approach to assess trends in river nutrient export by examining the effect of multiple factors (e.g., agricultural nutrient management, sewage treatment, socioeconomic trends, and food consumption). The goal is to improve water quality in freshwater ecosystems upstream of coastal waters, although it is important to manage water quality along the entire freshwater to marine continuum.
Several factors modulate the link between eutrophication and severity of hypoxia (e.g., land runoff, nutrient inputs, water column stratification, primary productivity, and microbial decomposition of organic matter) [17] [62] [81]. These factors are influenced by climate change through increases in temperature, storm activity, precipitation, wind action, sea level rise, acidification, and other variables, which then affect oxygen availability and ecological responses to hypoxia, as observed by Altieri and Gedan [69]. The additive, synergistic, or antagonistic interactions of multiple physical-chemical-biotic factors and climatic drivers that affect hydrologic and nutrient loading complicate the study of eutrophication development in estuarine and coastal marine ecosystems [6] [19]. However, detailed investigations indicate that climate change is facilitating coastal eutrophication and the increase in severity and expansion of hypoxic zones [39] [41] [58] [117] [118].
7. Hypoxia Link
Increasing human population growth along coasts, watershed urbanization, industrialization, and agricultural intensification over the past 50 years have had far-reaching effects on increased nutrient and organic matter loading and hypoxia development in estuarine and coastal marine waters. Dissolved oxygen is a keystone molecule in estuarine and coastal marine environments because of its critical role in the functioning of ecosystem processes, such as the production and decomposition of organic matter and the cycling of inorganic substances [10]. Hypoxia and anoxia develop in estuarine and coastal marine waters when oxygen sinks exceed oxygen sources, being driven by organic matter supply, respiration of the organic matter by microbes and metazoans, and the microbial oxidation of reduced inorganic species (e.g., ammonium and hydrogen sulfide) [119]. Hence, the mineralization of organic matter in and on bottom sediments and the remineralization of nutrients into the water column stimulate additional production of organic matter and the persistence of hypoxia or anoxia, most notably in bottom waters. Warming waters linked to climate change also promote deoxygenation of coastal waters by decreasing the solubility of oxygen in seawater, while concurrently increasing vertical stratification and oxygen consumption [119].
Physical processes play a significant role as well, with larger seasonal increases in the frequency and volume of freshwater inputs contributing to stronger density stratification that hinders vertical mixing of the water column and nutrient loading at depth. Hypoxia is more likely to occur when organic matter supply and transport to bottom waters are high, water residence time is protracted, and water exchange and ventilation are minimal [40]. Areas of hypoxia often underlie highly productive upwelling zones in coastal waters characterized by algal blooms and high accumulation of organic matter in bottom sediments [10] [17]. Increased wind forcing and reduced freshwater inputs occurring at least seasonally typically terminate water column stratification and increase vertical mixing and the resupply of oxygen, subsequently reducing hypoxia/anoxia occurrence.
While excess nutrient enrichment is a primary driver of eutrophication and deoxygenation, physical drivers that limit reaeration of bottom water also play a significant role in hypoxia formation [41]. Warming of bottom waters affects dissolved oxygen levels, particularly in regions where the water column is stratified in summer, such as in Chesapeake Bay [10] and some coastal waters in the UK and elsewhere [120]. Hypoxia reduces habitat availability and can be physiologically challenging or lethal to many estuarine and marine organisms. Greater frequency of extreme events (e.g., storms, floods, and droughts) affects organism responses, as does the generation time of the affected organisms, amounting to hours to days for phytoplankton, months to years for benthos, and years to decades for fish [95].
Depleted dissolved oxygen levels are hazardous to biotic communities, particularly in the benthos where organic matter accumulates and microbial decomposition predominates [41]-[43] [58]. Nutrients regenerated by mineralization in bottom sediments create biogeochemical feedbacks that increase the availability of both nitrogen and phosphorus in the water column that fuels additional phytoplankton and macrophyte production, which can accelerate eutrophication and expansion of hypoxia/anoxia along the seafloor [59] [77] [103] [112]. In contrast, denitrification and anaerobic ammonium oxidation (anammox) in bottom sediments result in a net loss of bioavailable nitrogen via the formation of dinitrogen gas (N2) [58].
As explained by Howarth et al. [77], even moderate increases in nutrient delivery and eutrophication in a highly stratified waterbody can result in hypoxic or anoxic conditions that are detrimental. In these impacted waters, benthic organisms typically exhibit increased mortality, decreased diversity, and altered reproduction, abundance, and distribution. The structure of benthic faunal communities exposed to eutrophic conditions with elevated supply of organic matter in bottom sediments often shift to dominance by pollution tolerant species [42]. Eutrophication is particularly problematic because it can also sustain frequent and intense destructive hypoxic events over extensive areas such as in the northern Gulf of Mexico [17] [43]. Here, high nitrogen loads discharged from the Mississippi River (USA), together with physical dynamics on the continental shelf that support vertical stratification, create conditions for oxygen stress and chronic hypoxia over areas that have exceeded 17,000 km2 [17] [40] [41] [59]. Other estuarine and coastal marine ecosystems with chronic hypoxia characteristically develop near altered watershed landscapes, where agricultural activity and runoff are intense [10].
The occurrence of oxygen-depleted dead zones has increased greatly in marine waters over the past 75 years, doubling every decade with greater eutrophication and climate change and causing devastating impacts on biotic communities and habitats globally [17] [40] [41] [43] [56] [69]. The effects in coastal waters have been most extreme, with Breitburg et al. [58] documenting more than 500 hypoxic sites (oxygen concentrations ≤2 mg liter−1 (=63 mmol liter−1 or ≅61 µmol·kg−1) since 1950. They reported that fewer than 10% of these coastal ecosystems were hypoxic prior to 1950. Between 1995 and 2007 alone, Diaz and Rosenberg [43] identified 405 dead zones affecting a total area of 247,000 km2. Hypoxic zones in estuarine and marine waters typically expand during the summertime, as is evident in the Chesapeake Bay, northern Gulf of Mexico, Baltic waters, German Bight, Danish coast, and Adriatic Sea.
Increased alteration of coastal wetlands over the past 50 years due to agricultural expansion and urban development, levee construction, modified hydrologic pathways, and escalating climate change have accelerated eutrophication and worsened hypoxia in nearby waters. Similar observations have been made in other coastal ecosystems. For example, Paerl et al. [116] showed that eutrophication has been problematic in the San Francisco Bay Delta (USA), where the natural hydrologic system has been significantly altered by channelization, dam construction, freshwater diversions, and levees in conjunction with chronic freshwater withdrawal. While human-altered hydrologic systems are common in coastal regions worldwide, there are few examples of the recovery of heavily impacted estuarine and coastal marine ecosystems from eutrophication and hypoxia that have developed in part from the hydrologic modifications.
The co-occurrence of eutrophication, climate change, and hypoxia poses a threat to the sustainability of estuarine and coastal marine ecosystems [69]. As population growth, watershed development, and human activities expand in coastal regions during the 21st century, efforts by management programs to maintain viable and sustainable estuarine and coastal marine ecosystems will be challenged [10]. Effective management programs are necessary to protect and conserve these vitally important ecosystems.
8. Management Controls
Rabalais et al. ([74], p. 1535) concluded more than 15 years ago that “Coastal water quality is currently on the decline.” They attributed the observed decline to the effects of escalating human population growth in coastal regions, more intense urbanization and industrialization, expanding agricultural activity, and global climate change, which were increasing eutrophication development as well as the frequency, severity, and extent of hypoxia in estuarine and coastal marine waters. They indicated that greater nutrient loads in these waters due to an array of human activities were an important driver of change and a key link between eutrophication occurrence and hypoxia formation. More specifically, they documented that climatic-driven higher water temperatures, increased nutrient-enriched freshwater flows, and stronger water column stratification were significantly affecting coastal ecosystems around the globe. Since then, additional studies have shown conclusively that, due to a multitude of interactive natural and anthropogenic drivers of change in these environments, it is not reliable to view coastal environmental degradation or management approaches strictly through a singular lens of land-based sources of impacts. In fact, the assessment of coastal environmental conditions and the management strategies necessary to remediate anthropogenic impacts on them are most effective when conducted using a holistic, multidisciplinary integrated approach that couples ecological, physical, and socio-economic systems for the protection and sustainability of these complex environments [101]. Solutions go beyond scientific intervention to include necessary societal controls or changes in culture [18] [24] [25] [101].
Eutrophication and hypoxia in estuarine and coastal marine waters are among the most serious coastal environmental concerns today. That they are exacerbated by escalating climatic drivers of change raises the concerns to a higher level. These pernicious problems can be mitigated greatly or even reversed by implementing long-term, broad-scale, and persistent efforts to reduce nutrient loads [17]. The reduction of nutrient loading is a key factor in circumventing the damaging effects of eutrophication and globally expanding hypoxia [7] [40].
Climatic drivers of change act on the most extensive temporal and spatial scales relative to other anthropogenic stressors, and the deleterious effects resulting from the multiple interactions of these factors in estuarine and coastal marine ecosystems are challenging to management programs tasked with remediating their ecological impacts [100] [101]. These management programs are in place to ensure that biodiversity is maintained and that the structure and function of the ecosystems are sustainable [26]. While a primary goal of the programs is to maintain coastal ecosystems in a healthy, productive, and resilient state, an additional goal is to concurrently protect delivery of ecosystem services and societal goods and benefits derived from them for human use [6] [18] [21]. This can be achieved most effectively by implementing an ecosystem-based management approach involving the collective application of management programs, governance (i.e., administration, policies, and legislation), and sustainable development plans that rely on an interplay of science, technology, and societal elements. It should consist of an integrated holistic design in which humans are also part of the whole ecosystem being investigated [11] [18] [23] [24] [26]. Recently, Borja et al. [22] developed a comprehensive conceptual framework model within an ecosystem-based management approach that advances the knowledge base on the cumulative effects of multiple pressures on estuarine and marine ecosystems and their services and promotes sustainable use of the ecosystems.
Difficulties of managing estuarine and coastal marine environments are ascribed to the complex driver interactions that impact the ecological structure and function of ecosystems, the variable physico-chemical processes therein, and the socio-economic components that must be considered as well [18] [24] [26] [37]. A highly successful management approach that addresses the causes, consequences, and responses to impacts has existed in various forms since the early 1990s. The most recent version is the cyclical DAPSI(W)R(M) framework (i.e., Drivers-Activities-Pressures-State Change-Impact-Responses-Recovery), which integrates relationships between human activities, their pressures and impacts to the environment, and the management responses with solutions to the deleterious effects [18] [24] [71]. Specific elements of this framework include the following: Drivers (human needs, activities, and the economic sectors responsible for the environmental pressures), Pressures (particular stressors on the environment), State (the characteristics and conditions of the environment), Impacts (effects on human welfare due to changes in the natural and human system and the ways in which humans use the estuarine and marine areas), Responses (management measures used and the creation of different policy options and economic instruments to overcome the state changes and impacts), and Recovery (a reduction in the state changes as a result of these actions which may include restoration as an integral component) [18]. Each DAPSI(W)R(M) cycle relates to a particular Driver or human activity in which the management unit is the estuarine or coastal marine ecosystem.
Another useful management strategy for supporting healthy estuarine and coastal marine environments and for sustaining services to society is ecosystem-based marine spatial planning, which informs the spatial distribution of activities in an area [72] [121] [122]. It is a valuable strategic instrument for dealing with conflicting spatial use of marine resources [72]. According to Foley et al. ([123], p. 956), an important element of this management strategy is to “maintain the delivery of valuable ecosystem services for future generations in a way that meets ecological, economic, and social objectives.” Ecological principles are incorporated into the applications to ensure healthy functioning ecosystems and biodiversity conservation, while also contributing to sustainable economic and societal benefits. Recently, Galparsoro et al. [11] developed a useful assessment framework and tool that integrates fundamental principles of an ecosystem approach to management that addresses the implementation challenges of ecosystem-based management principles in marine spatial planning processes. Furthermore, Papadopoulou et al. [124] identified 19 tool groups useful for application in the ecosystem-based management context.
Anthropogenic activities cause pressures that are often detrimental to estuarine and coastal marine environments [125]. They are subject to and can contribute to hazards that become risks when something of value to humans is adversely affected [18]. An example is overfishing that causes a decline of fisheries, or the input of contaminants that impairs water quality. This is why socio-economic factors are also important in assessing and managing the condition of estuarine and coastal marine ecosystems.
9. Conclusions
Climate change is a major forcing factor modulating ecosystem processes in estuarine and coastal marine environments. Climate change drivers interact additively, synergistically, or antagonistically with multiple non-climatic anthropogenic stressors to alter physico-chemical conditions and biotic communities in these environments. The impact of climate change on coastal environments has progressively increased since the mid-20th century with rising global mean temperature resulting in the modification of ecosystem structure and function and the loss of ecosystem services of value to humankind. Coastal ecosystems are thus in a state of flux driven by climatic forcings that are causing a paradigm shift in the assessment and management of these vital environments. This article examines the interaction of climate change drivers and eutrophication as an example of how significant the resulting impacts are on estuarine and coastal marine environments. The main conclusions are as follows:
1) Eutrophication is an insidious degrading environmental condition caused by an increase in the rate of organic matter supply to an ecosystem and the development of undesirable consequences that pose a threat to its structure and function. The deleterious impacts of eutrophication are on the rise because of greater anthropogenic alteration of coastal watersheds, accelerated nutrient and organic matter inputs, and climate change.
2) Symptoms of eutrophication include an array of cascading environmental problems such as HABs, impaired water quality, loss of essential habitat (e.g., seagrasses, mangroves, salt marshes, and shellfish beds), reduced biodiversity, species distributional shifts, altered biotic communities, declining harvestable fisheries, imbalanced trophic food webs, oxygen depletion (hypoxia and anoxia), and diminished ecosystem resilience.
3) In shallow estuaries, eutrophication causes a shift in macrophyte dominance from seagrasses and perennial macroalgae to ephemeral, bloom-forming macroalgae and epiphytes leading to significant changes in biotic communities.
4) Nutrient enrichment and organic matter loading in estuarine and coastal marine environments emerged as an escalating ecological problem after 1950 due to increasing human population growth and development in coastal regions and the greater influence of climate change, which has become more impactful in recent decades driven by higher global mean temperature.
5) Allochthonous and autochthonous inputs of organic matter in estuarine and coastal marine environments are increasing with greater influence of climate change.
6) Anthropogenic climatic forcings, primarily those factors linked to an inability to curb greenhouse gas emissions (notably carbon dioxide, nitrous oxides, and methane), as well as deforestation and watershed land-use and land-cover changes, have increased air and water temperatures and altered biogeochemical cycling and other coastal processes.
7) The interaction of climate change forcings and eutrophication exacerbates adverse effects on the structure and function of estuarine and coastal marine biotic communities.
8) Increased storm intensity and precipitation, land runoff, river discharges, and warming driven by climate change are leading to greater nutrient delivery and organic matter loading, enhanced thermal and salinity stratification, altered water circulation, increased algal blooms, light attenuation in the water column, biogeochemical and trophodynamic changes, and deteriorated sediment and water quality in estuarine and coastal marine ecosystems.
9) The frequency, intensity, and extent of hypoxia are increasing in estuarine and coastal marine environments where climate change amplifies the effects of eutrophication.
10) Hypoxia and anoxia of bottom waters have devastating impacts, often resulting in extensive loss of estuarine and marine life in benthic communities, fisheries declines, as well as damage to habitats.
11) The co-occurrence of climate change, eutrophication, and hypoxia poses a threat to the viability and sustainability of estuarine and coastal marine environments.
12) A primary goal of estuarine and coastal marine management programs is to maintain coastal ecosystems in a healthy, productive, and resilient state, and to protect sustainable delivery of ecosystem services and societal goods and benefits derived from them for human use. To effectively assess and remediate the impacts of eutrophication and climate change for long-term protection and sustainability of these environments, a holistic integrated and unifying management framework is required to address the causes, consequences, and responses to the impacts. In this respect, the cyclical DAPSI(W)R(M) framework (i.e., Drivers-Activities-Pressures-State Change-Impact-Responses-Recovery) is a highly successful management approach that has existed since the early 1990s. It integrates relationships between human activities, their pressures and impacts on the environment, and the management responses with solutions to the deleterious effects.
Acknowledgements
This is Contribution Number 5248 of the Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, New Jersey (USA).