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The Growing Human Footprint on Coastal and Open-Ocean Biogeochemistry

 

The Growing Human Footprint on Coastal and Open-Ocean Biogeochemistry

Science, June 18, 2010  
 
Climate change, rising atmospheric carbon dioxide, excess nutrientinputs, and pollution in its many forms are fundamentally alteringthe chemistry of the ocean, often on a global scale and, insome cases, at rates greatly exceeding those in the historicaland recent geological record. Major observed trends includea shift in the acid-base chemistry of seawater, reduced subsurfaceoxygen both in near-shore coastal water and in the open ocean,rising coastal nitrogen levels, and widespread increase in mercuryand persistent organic pollutants. Most of these perturbations,tied either directly or indirectly to human fossil fuel combustion,fertilizer use, and industrial activity, are projected to growin coming decades, resulting in increasing negative impactson ocean biota and marine resources.
 
 
Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA. E-mail: sdoney@whoi.edu
 
 
The ocean plays a pivotal role in the global biogeochemicalcycles of carbon, nitrogen, phosphorus, silicon, and a varietyof other biologically active elements and chemical compounds(1, 2). Human fossil-fuel combustion, agriculture, and climatechange have a growing influence on ocean chemistry, both regionallyin coastal waters and globally in the open ocean (35)(Fig. 1). Some of the largest anthropogenic impacts are on inorganiccarbon (6), nutrients (4, 7), and dissolved oxygen (8, 9), whichare linked through and affect biological productivity. Seawaterchemistry is also altered, some times quite strongly, by theindustrial production, transport, and environmental releaseof a host of persistent organic chemicals (10) and trace metals,in particular mercury (11), lead (12), and perhaps iron (13).
 
Marine biogeochemical dynamics is increasingly relevant to discussionsof ecosystem health, climate impacts and mitigation strategies,and planetary sustainability. Human-driven chemical perturbationsoverlay substantial natural biogeochemical cycling and variability.Key scientific challenges involve the detection and attributionof decadal and longer trends in ocean chemistry as well as moredefinitive assessments of the resulting implications for oceanlife and marine resources.
 
The biogeochemical state of the sea reflects both cycling andtransformations within the ocean, much of which are governedby biological dynamics, and fluxes across the ocean boundarieswith the land, atmosphere, and sea floor (2, 14). For most chemicalspecies, seawater concentrations are governed more by kinetics—therates of net formation and transport processes—than bychemical equilibrium with particles and sediments. Clear exceptionsare dissolved gases such as carbon dioxide (CO2) and oxygen(O2), which are driven to solubility equilibrium with the partialpressure of gases in the atmosphere in the surface ocean byair-sea gas exchange.
 
Phytoplankton in the ocean surface plays a crucial biogeochemicalrole, converting CO2 and nutrients into particulate organicand inorganic matter via photosynthesis and releasing O2 inthe process. The rate of marine primary production is governedby temperature, light (strongly influenced by surface turbulentmixing depths), and limiting nutrients, most notably nitrogen,phosphorus, iron, and silicon for some plankton. Some fractionof the biologically produced particulate matter subsequentlysinks into the subsurface ocean and is consumed by microbesand macrofauna, releasing CO2 and nutrients and consuming subsurfaceO2. Export production thus maintains strong vertical gradientsin biogeochemical tracers over the water column.
 
The global biologically driven export flux of ~10 Pg of C year–1 must be balanced by a supply of "new" nutrients brought up frombelow by ocean circulation, input by rivers, or deposited fromthe atmosphere. With sufficient iron and phosphorus, some diazotrophicmicrobes can produce "new" nitrogen in situ through nitrogenfixation that converts inert nitrogen gas into biological reactivenitrogen. Marine microbes produce and consume a number of tracegases that can influence climate, for example CO2, nitrous oxide(N2O), methane (CH4), and dimethylsulfide (DMS).
Ocean upwelling and mixing bring water with elevated CO2 andnutrients to the surface and replenish subsurface O2, with ventilationtime scales of years to a few decades in the main thermocline(upper 1 km of the water column) and many centuries for deepwaters. Natural ocean-atmosphere climate modes (e.g., El Nino–SouthernOscillation and Pacific Decadal Oscillation) generate substantialinterannual to interdecadal variability in ocean biogeochemistry.The major external source terms to the ocean are typically riverinputs and atmospheric deposition of dust, aerosols, and precipitation.These source terms are balanced mostly by losses to the seafloorvia the burial of the small fraction (<1% of organic matter)of sinking particulate matter that is not destroyed either inthe water column or in surface sediments.
 
Human Drivers on Biogeochemical Cycles and Ocean Climate
 
For most of history, it was inconceivable that humankind coulddirectly influence ocean chemistry other than in local and inconsequentialmanners. That changed after the industrial revolution with thedevelopment of modern energy systems, chemical industries, andagriculture that process ever-growing volumes of material, someof which are released either advertently or inadvertently intothe environment and eventually reach the ocean. For example,because of human fossil-fuel combustion, deforestation, andland-use change (3), global mean atmospheric carbon dioxide(CO2) has grown by almost 40% from about 280 parts per million(ppm) in the preindustrial era to nearly 388 ppm by 2010 (15).The invention of the Haber-Bosch process, which converts N2gas into fixed nitrogen for agricultural fertilizer, has hadan even greater proportional impact on the global nitrogen cycle,approximately equaling the annual production of reactive nitrogenfrom natural sources (4). Comparable amplifications of a factorof 2 to 3 have occurred in the emissions of reactive phosphorus(16) and mercury (17) to the atmosphere and hydrosphere.
 
Indirect human effects on ocean chemistry can also occur, mainlythrough climate change. According to the most recent synthesisby the Intergovernmental Panel on Climate Change, warming ofthe climate system since the mid-20th century is unequivocaland is very likely caused by the increase in anthropogenic greenhousegas concentrations (CO2, N2O, CH4, and chlorofluorocarbons)(18). Documented physical changes relevant to ocean biogeochemistryinclude upper-ocean warming, altered precipitation patternsand river runoff rates, and sea-ice retreat in the Arctic andthe West Antarctic Peninsula. Reduced stratospheric ozone overAntarctica appears to be causing a major shift in atmosphericpressure (more positive Southern Annular Mode conditions), whichstrengthens and displaces poleward the westerly winds in theSouthern Ocean and which also may be increasing ocean verticalupwelling (19). Future climate projections indicate continuation,and in many cases acceleration, of these trends as well as otherchanges such as more intense tropical storms, an ice-free summerin the Arctic, and a very likely reduction in the strength ofthe Atlantic deepwater formation.
 
Ocean Uptake of Anthropogenic CO2
 
Rising atmospheric CO2 causes a net air-to-sea flux of excessCO2 that dissolves in surface seawater as inorganic carbon throughwell-known physical-chemical reactions. The global uptake rateis governed primarily by atmospheric CO2 concentrations andthe rate of ocean circulation that exchanges surface watersequilibrated with elevated CO2 levels with subsurface waters.The distribution, global inventory, and decadal trend in anthropogenicCO2 are well characterized from ship-based observations (6,20) and models (3). Based on a recent synthesis, in 2008 fossil-fuelcombustion released 8.7 ± 0.5 Pg of C year–1 tothe atmosphere primarily as CO2, contributing to an ocean uptakeof 2.3 ± 0.4 Pg of C year–1 (3). Cumulative oceancarbon uptake since the beginning of the industrial age is equivalentto about 25 to 30% of total human CO2 emissions (6).
 
Climate change is expected to decrease ocean uptake of anthropogenicCO2 because of lower CO2 solubility in warmer waters and slowerphysical transport into the ocean interior due to increasedvertical stratification and reduced deepwater formation (21).In contrast, stronger Southern Ocean winds and ocean upwellingmay increase future uptake of anthropogenic CO2 (22). Changesin ocean circulation also alter the upward transport of subsurfacewater enriched in nutrients and dissolved inorganic carbon,and these biogeochemical feedbacks tend to partially offsetclimate effects on anthropogenic CO2 uptake. In model estimatesfor the contemporary Southern Ocean for example, enhanced effluxof natural CO2 due to stronger winds and upwelling more thancompensates for increased anthropogenic CO2 uptake, leadingto a net reduction in global ocean uptake (19, 23). Recent observationsof the air-sea difference in the partial pressure of carbondioxide (pCO2), the driving force for air-sea CO2 exchange,indicate a weakening of oceanic uptake in a number of regions,although there remains some debate about whether this signalshould be attributed primarily to climate change or decadalclimate variability (3, 24).
 
Ocean Acidification
 
Ocean uptake of anthropogenic CO2 also alters ocean chemistry,leading to more acidic conditions (lower pH) and lower chemicalsaturation states ({Omega}) for calcium carbonate (CaCO3) mineralsused by many plants, animals, and microorganisms to make shellsand skeletons (25). Seawater acid-base chemistry is bufferedlargely by the inorganic carbon system, and CO2 acts as a weakacid in seawater. Processes that add CO2, like air-to-sea gasflux or bacterial respiration of organic matter, increase theconcentration of hydrogen ions (H+) and thus decrease pH (pH= –log10[H+]).
 
Critically for many organisms, the addition of CO2 reduces carbonateion (CO32–) concentration through the reaction H+ + CO32– ->HCO3, even though the total amount of dissolved inorganiccarbon (DIC) goes up (DIC = [CO2] + [H2CO3] + [HCO3]+ [CO32–]). Declining CO32– in turn lowers CaCO3saturation state, {Omega}= [Ca2+][CO32–]/Ksp, where Ksp is thethermodynamic solubility product that varies with temperature,pressure, and mineral form. Ocean surface waters are currentlysupersaturated ({Omega} > 1) for the two major forms used by marineorganisms, aragonite (corals and many mollusks) and calcite(coccolithophores, foraminifera, and some mollusks). Becauseof pressure effects and higher metabolic CO2 from organic matterrespiration, {Omega}decreases with depth, often becoming undersaturated({Omega} < 1), at which point unprotected shells and skeletons beginto dissolve.
 
Ocean acidification is documented clearly from ocean time-seriesand survey measurements over the past two decades (Fig. 2) (26, 27). From preindustrial levels, contemporary surface oceanpH has dropped on average by about 0.1 pH units (a 26% increasein [H+]), and additional declines of 0.2 and 0.3 pH units willoccur over the 21st century unless human CO2 emissions are curtailedsubstantially (28). Surface ocean CaCO3 saturation states aredeclining everywhere, and polar surface waters will become undersaturatedfor aragonite when atmospheric CO2 reaches 400 to 450 ppm forthe Arctic and 550 to 600 ppm for the Antarctic (29). Subsurfacewaters will also be affected but more slowly, governed by oceancirculation, with the fastest rates in the main thermoclineand high latitudes where cold surface waters sink into the oceaninterior. Many coastal waters naturally have low pH, a factoramplified by acid rain (30) and nutrient eutrophication (seebelow).
The rates of change in global ocean pH and {Omega}are unprecedented,a factor of 30 to 100 times faster than temporal changes inthe recent geological past, and the perturbations will lastmany centuries to millennia. The geological record does containpast ocean acidification events, the most recent associatedwith the Paleocene-Eocene Thermal Maximum 55.8 million yearsago. But these events may have occurred gradually enough andunder different enough background conditions for ocean chemistryand biology that there is no good paleo-analog for the currentsituation (31).
 
On the basis of laboratory experiments and limited surveys acrossocean chemistry gradients, ocean acidification will likely reduceshell and skeleton growth by many marine calcifying speciesincluding corals and mollusks (25). Ocean acidification alsomay reduce the tolerance of some species to thermal stress.Some studies suggest a threshold of about 550 ppm atmosphericCO2 where coral reefs would begin to erode rather than growbecause of acidification and surface ocean warming; this wouldnegatively affect diverse reef-dependent taxa (32). Polar ecosystemsalso may be particularly susceptible when surface waters becomeundersaturated for aragonite, the mineral form used by many mollusks.
 
Some organisms may benefit in a high-CO2 world, in particularphotosynthetic organisms that are currently limited by the amountof dissolved CO2 in seawater. In laboratory experiments withelevated CO2, higher photosynthesis rates are found for certainphytoplankton species, seagrasses, and macroalgae, and enhancednitrogen-fixation rates are found for some cyanobacteria. Indirectimpacts on noncalcifying organisms and marine ecosystems asa whole are possible but more difficult to characterize frompresent understanding.
 
Climate Change and Trends in Biological Productivity
 
Primary production by upper-ocean phytoplankton forms the baseof the marine food web and drives ocean biogeochemistry throughthe export flux of organic matter and calcareous and siliceousbiominerals from planktonic shells. Satellite observations indicatea strong negative relationship, at interannual time scales,between productivity and warming in the tropics and subtropics,most likely because of reduced nutrient supply from increasedvertical stratification (33). Numerical models project declininglow-latitude marine primary production in response to 21st-centuryclimate warming (34). The situation is less clear in temperateand polar waters, although there is a tendency in models forincreased production because of warming, reduced vertical mixing,and reduced sea-ice cover. The climate signal in primary productionmay be difficult to distinguish from natural variability formany decades (35).
 
Changes in atmospheric nutrient deposition also can alter productivitybut mostly on regional scales near industrial and agriculturalsources. Present anthropogenic reactive nitrogen depositionto the surface ocean (54 ± 23 Tg of N year–1) (Fig. 3) supports an export production of ~0.3 Pg of C year–1 (~3% of global total) while producing an additional ~1.6 Tgyear–1 of N2O (7). In much of the North Pacific, equatorialPacific, and Southern Ocean, phytoplankton are limited by iron,but most of the atmospheric iron deposition is in the form ofmineral dust that is not readily bioavailable. Anthropogeniccombustion sources and increased cloud-water acidity are increasingsoluble iron input to the ocean (13, 36). Models suggest thatanthropogenic iron deposition could have a greater positiveimpact on productivity than anthropogenic nitrogen and alsoenhance nitrogen fixation, but direct observations are lacking(37).
 
Coastal Hypoxia and Open-Ocean Deoxygenation
 
Low subsurface O2, termed hypoxia, occurs naturally in open-oceanand coastal environments from a combination of weak ventilationand/or strong organic matter degradation (8, 9). Dissolved O2gas is essential for aerobic respiration, and low O2 levelsnegatively affect the physiology of higher animals, leadingto so-called "dead-zones" where many macrofauna are absent.Thresholds for hypoxia vary by organism but are ~60 µmolof O2 kg–1 or about 30% of surface saturation. Under suboxicconditions (<5 µmol kg–1), microbes begin touse nitrate (NO3) rather than O2 as a terminal electron acceptorfor organic matter respiration (denitrification), resultingin reactive nitrogen loss and N2O production. Toxic hydrogensulfide (H2S) production occurs under anoxic (no O2) conditions.The organic matter respiration that generates hypoxia also elevatesCO2, thus leading to coupled deoxygenation and ocean acidificationin a future warmer, high-CO2 world. The synergistic effectsof these multiple stressors may magnify the negative physiologicaland microbial responses beyond the impacts expected for eachperturbation considered in isolation (38, 39).
 
Fertilizer runoff and nitrogen deposition from fossil fuelsare driving an expansion in the duration, intensity, and extentof coastal hypoxia, leading to marine habitat degradation and,in extreme cases, extensive fish and invertebrate mortality(8, 40, 41). About half the global riverine nitrogen input (50to 80 Tg of N year–1) is anthropogenic in origin (4, 42),and anthropogenic nitrogen deposition is concentrated in coastalwaters downwind of industrial and intensive agricultural regions(30). The result is coastal eutrophication and enhanced organicmatter production, export, and subsurface decomposition thatconsumes O2. Nutrient eutrophication is also associated withincreased frequency of harmful algal blooms (43).
 
Worldwide there are now more than 400 coastal hypoxic systemscovering an area > 245,000 km2 (40). Population growth andfurther coastal urbanization will only exacerbate coastal hypoxiawithout careful land and ocean management. Accelerated hypoxiamay also result from climate warming and regional increasesin precipitation and runoff that increase water-column verticalstratification; on the other hand, more intense tropical stormscould disrupt stratification and increase O2 ventilation (8).
 
Expanding coastal hypoxia is also induced in some regions byreorganization in ocean-atmosphere physics. Off the Oregon-Washingtoncoast, increased wind-driven upwelling is linked to the firstappearance of hypoxia, and even anoxia, on the inner shelf after5 decades of hypoxia-free conditions (44). Further south inthe California Current System, the depth of the hypoxic surfacehas shoaled along the coast by up to 90 m (45). The same physicalphenomenon, along with the penetration of fossil-fuel CO2 intooff-shore source waters, are introducing waters corrosive toaragonite ({Omega} < 1) onto the continental shelf (46). There isconflicting evidence on how coastal upwelling may respond toclimate change, and impacts may vary regionally (47).
 
Extensive deoxygenation is also occurring in the open ocean,most notably in the thermocline of the North Pacific and tropicaloceans (9, 48) (Fig. 4). A portion of the observed oxygen changelikely reflects decadal variability in ocean circulation, butsimilar to ocean CO2 distinct secular trends are apparent atsome long-term time series stations (49). Models project furtherreductions of 1 to 7% in the global oxygen inventory and expansionsof open-ocean oxygen minimum zones over the 21st century fromdecreased solubility in warmer waters and slower ventilationrates (50).
 
The Global Spread of Industrial Pollutants
 
Points sources of pollution from industrial discharges and oilspills are often highly visible and destructive to the localand regional marine environment (51). Perhaps less well knownis the global spread of industrial pollutants into what otherwisewould appear to be pristine environments. Elevated oceanic levelsof persistent organic pollutants (10) and methyl mercury, ahighly toxic organic form (11), raise serious concerns for marineecosystem health and, potentially, human health through theconsumption of contaminated seafood. Many organic and organo-metalliccompounds bioaccumulate in the fatty tissues of marine organismsat levels orders of magnitude higher than ambient seawater concentrations.Such pollutants are passed up the food chain and are most concentratedin marine organisms at the higher trophic levels including predatoryfish, marine mammals, and seabirds.
 
Key factors in determining overall biological impacts for aparticular pollutant are source magnitudes and locations, physicaland biological transport pathways, toxicity, and persistencein the environment. Pollutants exhibit elevated levels nearlocal point sources and in coastal and open-ocean waters becauseof atmospheric deposition downwind of industrial regions (e.g.,western Pacific near East Asia and North Atlantic near NorthAmerica and Western Europe) (17, 52) (Fig. 3). However, theyare also distributed globally, found in even the most remotemarine locations, transported through the atmosphere in thevapor phase, aerosols, and soot particles (i.e., black carbon);by ocean currents; and in some cases by migrating animals (53).
 
Elemental mercury (Hg0), the main chemical form in the ocean,is transformed into the more toxic methyl mercury form by microbes,particularly in reduced environments such as coastal sedimentsand perhaps oxygen minimum zones (11). Although mercury distributionsare poorly characterized from direct seawater measurements,time histories reconstructed from numerical models (17) andbiological samples (e.g., seabird feathers) indicate increasingtrends over the 20th century (11). It is encouraging that, afterthe phaseout of leaded gasoline in North America that beganin the mid-1970s, the high levels of anthropogenic lead observedin the North Atlantic declined sharply and are now comparableto those occurring at the beginning of the 20th century (12).
 
Some persistent organic pollutants are synthetic and did notexist in nature before industrial manufacture. Production forsome organic pollutants peaked in developed nations in the mid-to late 20th century but is continuing to grow in the developingworld. Commonly measured synthetic contaminants include pesticideslike DDT, polychlorinated biphenyls, and brominated flame retardantssuch as polybrominated diphenyl ethers. However, there are manymore organic compounds synthesized and used that presumablyexist in the ocean but that have not been detected (54).
 
Human activities have also increased levels of naturally occurringcompounds such as polycyclic aromatic hydrocarbons, which havesources from petroleum spills and natural oil seeps as wellas, primarily, incomplete combustion from wildfires, biomassburning, and fossil fuels (55). In a study on the Gulf of Mainedownwind of the Northeast United States, another combustionproduct, black carbon, contributed up to 20% of the total particulateorganic carbon in seawater and about half of the "molecularlyuncharacterized" fraction (56). Environmental samples oftencontain organic compounds similar in chemical structure to knownpollutants but which may be biosynthesized natural products;compound-specific radiocarbon analysis is emerging as a powerfultool for distinguishing between natural and industrial sources(10).
 
Future Research Directions
 
A deeper understanding of human impacts on ocean biogeochemistryis essential if the scientific community is to provide appropriateand timely information to the public and decision-makers onpressing environmental questions. Although some progress hasbeen made on a nascent ocean observing system for CO2 (57),the marine environment remains woefully undersampled for mostcompounds. The oceanographic community needs to develop a coordinatedobservational plan that takes better advantage of in situ autonomoussensors and observation platforms (58). Monitoring efforts shouldbe paired with laboratory and field process studies to betterelucidate the biological effects of changing chemistry at organism,population, and ecosystem levels.
 
In particular, more detailed biochemical, system biology, andgenomic studies are required to explain mechanistically theresponses of cells and organism to external perturbations, supplementingwhat have often been to date more phenomenological findings.Genomic and physiological research should be embedded in large-scaleecological and biogeochemical spatial surveys and time seriesto facilitate scaling to ecosystems (59). Further work is neededacross scales exploring possible synergistic effects among multiplestressors and to assess the potential for biological acclimationand adaptation to human perturbations over decadal to centennialtime scales. Lastly, targeted research is needed on the impactson marine resources and fisheries, potential adaptation strategies,and the consequences for human social and economic systems (60).
 
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  • 61. This work was supported by the Center for Microbial Oceanography, Research and Education (C-MORE) (NSF grant EF-0424599) and the W. Van Alan Clark, Sr. Chair for Excellence in Oceanography from the Woods Hole Oceanographic Institution. I thank J. Dore for Fig. 2, I. Lima for Fig. 3, S. Mecking for Fig. 4, and C. Reddy and C. Lamborg for discussions on ocean pollutants.
http://www.sciencemag.org/cgi/content/full/328/5985/1512