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Ocean Oxygen – another climate shoe dropping

Posted on 18 May 2016 by howardlee

How warming temperatures and ocean acidification are recreating an ancient killer

Ocean anoxia – widespread oxygen-starved dead zones in oceans - did the killing of ocean life in several mass extinctions of Earth’s past.  Anoxia went hand-in-hand with CO2 emissions, rising global temperatures, and (often) ocean acidification, a situation which today’s climate change is recreating with uncanny likeness.

Atmospheric oxygen levels are declining as a result of burning fossil fuels, but that’s not the cause of ocean anoxia. Neither are we at risk from asphyxiation, because the oxygen decline is at a rate of about 4 parts per million (ppm) per year, compared to an atmospheric oxygen concentration of 21% (ie 210,000 ppm). It would take nearly 4,000 years of burning fossil fuels at current rates before atmospheric oxygen declined to unsafe levels!

Even in normal, healthy oceans, dissolved oxygen levels in middle-depth waters (between about 500 to 1,500 meters) are low enough to discourage most higher animals. This makes those depths an important refuge for krill and other prey species to hang out during the day, safe from visual predators. In the dark of night, these creatures venture nearer the surface to graze on plankton, an impressive commute given their small size.

Dissolved oxygen in depth slices through our oceans

Depth slices through the oceans showing how dissolved oxygen declines from the surface to middle depths and then rises again in deep water. Constructed from World Ocean Atlas 2013.

There are places around the world where these oxygen minimum zones are much shallower than elsewhere, and there are also coasts where polluted river water delivers excess nutrients into the sea, causing coastal dead zones, for example in the Gulf of Mexico. But these pale in comparison to times in Earth’s past when ocean anoxia became so intense and widespread that it contributed to the permanent annihilation of many marine species. But if we look at the conditions that led to past “Ocean Anoxic Events” (OAEs), and compare them to our altered climate in the coming decades, the parallels are sobering.

How it works:

There is a complex interplay between a warming climate, its effects on land, delivery of nutrients to the ocean, life’s response to the changes, and chemical results. It works mainly by affecting 2 complementary parts of the ocean carbon cycle:

  1.       the biological carbon pump
  2.       the remineralization depth

The biological carbon pump is the process that transports carbon from the near-surface of the ocean to deep water. It is the overall effect of sinking fecal matter along with dead, decaying remains of near-surface life, hitchhiking microbes, and a broth of organic molecules. In this way the biological carbon pump takes carbon that was in the atmosphere before it was fixed into organic matter by photosynthesizing plankton, and sequesters it into the deep ocean and seafloor. For more detail on the biological carbon pump see this explainer by Nature Education.

Remineralization uses the carbon in the biological pump as food for myriad lifeforms, chiefly zooplankton and microbes, which convert it back to CO2 through respiration, consuming oxygen and liberating nutrients at the same time. Remineralization therefore works against the carbon pump. The remineralization depth is the depth to which most organic matter sinks before it is consumed and respired, determined by factors like the amount of shelly mineral, how clumped the organic particles are, how big they are, and how soluble they are. It’s not so much a single floor level but a diminishing curve, represented by the depth at which only 37% of the original organic matter remains (0.37≈ 1/e). In modern oceans it is about 590 meters deep.

Ocean anoxia and euxinia causes and feedbacks

The complex biogeochemical connections in ocean anoxia. The 3 connected drivers of anoxia include warming (left), acidification (center), and nutrient supply (right). This diagram is schematic, based partially on Gehlen et al in “Ocean Acidification”, OUP 2011, and on others referenced below.


Healthy oxygenated ocean for comparison to anoxic ocean

The stronger biological pump and deeper remineralization in a normal, pre-industrial ocean. This diagram is schematic, based partially on Gehlen et al in “Ocean Acidification”, OUP 2011, and on others referenced below.

Remineralization depth feedback to atmospheric CO2

A deep remineralization depth encourages oxygenated deep water and a strong carbon pump. It also increases the concentration of CO2 in deep water compared to shallow waters, so that where those waters eventually well up to the surface, they can cause localized CO2 outgassing back into the atmosphere, rather than absorbing CO2 from the atmosphere. A shallow remineralization depth, on the other hand, encourages oxygen-starved zones in relatively shallow water. It also liberates CO2 near the ocean surface, reducing the ocean’s ability to absorb atmospheric CO2.

During the last ice age the remineralization depth deepened by about 110 meters, reducing atmospheric CO2 by 30 – 77ppm, while modern warming of the oceans does the opposite - it moves the remineralization depth shallower, reducing the oceans’ CO2 absorption capacity, with potentially substantial impacts on atmospheric CO2 levels expected this century.

Some terminology:

Different words are used to describe different degrees of deoxygenation: “hypoxic,” “suboxic” and “anoxic” just refer to decreasing levels of dissolved oxygen. “Euxinic” describes waters that are not only anoxic but where sulfate-reducing bacteria are generating toxic hydrogen sulfide (the “rotten egg” gas). As oxygen levels decline, microbes use other chemicals, eg nitrate, to power their anaerobic respiration.






Oxygen level:

< ~60 μmol kg−1

<∼5 μmol kg−1,

<∼1 μmol kg−1,

<∼1 μmol kg−1,


dead zone for many higher animals

Anaerobic: Nitrate reduction

Anaerobic: Mn, Fe reduction

Anaerobic: Sulfate reduction and H2S production, Methane oxidation

Based on Keeling et al 2010 , Gilly et al 2013 , Wright et al 2012

Examples from Earth’s past.

Several of the big global warming events in Earth’s past were also Ocean Anoxic Events, with widespread ocean anoxia coupled to global warming, and, in most cases, ocean acidification –  like today.


Associated Large Igneous Province

Global Warming?

Marine Anoxia?

Ocean Acidification?



North Atlantic




Bond & Wignall 2014Babila et al 2016


Deccan (+ Chicxulub impact)




Mizukami et al 2013, De Oca et al 2013Thibault & Husson 2016

Coniacian-Santonian (Oceanic Anoxic Event 3: OAE-3)





Ji et al 2015

Cenomanian–Turonian (Oceanic Anoxic Event 2: OAE-2)

(a.k.a. “Bonarelli event”)





Du Vivier et al 2014 , Reolid et al 2016

Early Albian Oceanic Anoxic Event (OAE1b)





Erba et al 2015, Sabatino et al 2015

Aptian Ocean Anoxic Event (OAE 1a)

(a.k.a. “Selli event”)

Ontong Java




Naafs et al 2016, Erba et al 2015 Patruno et al 2015







Burgess et al 2015


Central Atlantic




Van de Schootbrugge & Wignall 2016

Carnian (Triassic)





Ruffell et al 2015, Dal Corso et al 2015


Siberian Traps




Lau et al 2016

Van de Schootbrugge & Wignall 2016







Bond et al 2015, Chen et al 2013







Bond & Wignall 2014,



Warming after intense cooling



Ghienne et al 2014






Bond & Wignall 2014Jourdan et al 2014


How it worked back then and today:


In all cases except the Ordovician, it started with rapidly rising CO2 levels (in most cases, if not all, from Large Igneous Province eruptions), which generated global warming. The warmer oceans and atmosphere promoted stronger chemical weathering of rocks, liberating their nutrients into rivers, which delivered them to lakes and oceans. For OAE-2 in the Cretaceous, chemical weathering is calculated to have increased by 300% in response to a 5ºC sea-surface warming.

Warming has a direct effect on deoxygenation because warmer water dissolves less gas, so warming reduces the amount of oxygen dissolved in oceans; but this is not nearly as strong a factor in creating ocean anoxia as the effect of nutrients (see below). Warming exerts a stronger effect by increasing ocean life’s metabolic rates, which typically double for every 10ºC increase in shallow oceans (ie doubling oxygen demand, so using up dissolved oxygen twice as fast). Warming also causes the remineralization depth to rise.

Deep ocean warming alters the population of bacteria and archaea (archaea look like bacteria but have different genetics and biochemistry) that live in deep ocean sediments. As water temperatures rise, the microbe population, especially of archaea, actually declines significantly. Since their habitat covers 65% of the globe, this population decline represents a significant change in the balance between carbon in water and carbon in sediments.

The combined effects of warming are to increase nutrient supply to oceans, raise the remineralization depth, increase the respiration rate, and reduce oxygen solubility – all of which reduce ocean oxygen concentration in progressively shallower waters.

Nutrient supply and trapping

The level of oxygen dissolved in water is overwhelmingly controlled by the supply of nutrients to the food web.

Phytoplankton (plant plankton, algae) and zooplankton (animal plankton) make up over 90% of the mass of marine life and form the base of the food web. If the supply of nutrients (including carbon, phosphate, Iron, nitrogen, etc) increases, it enables them to multiply and bloom. As they multiply, they excrete waste and they support the multiplication of life that feeds on them, which also excrete more waste. Most of that life respires using up oxygen, so as oceans support ever more plankton and microbial life, oxygen levels in shallow water drop substantially.

When Montiero et al (2012) ran models of the Cretaceous OAE-2 event, they were only able increase ocean anoxia by a couple of percent by reduced oxygen solubility alone, but when they added nutrients, the global oceanic oxygen decreased by 70% and the geographic areas of anoxia expanded from 5% to over 50%, matching the observations of the extent of anoxia in the geological record for that time.

Massive nutrient supply even seems to be able to generate anoxia in cold oceans. As the planet emerged from the last ice age, ocean anoxia expanded in the Eastern Pacific. A similar but far more extreme situation seems to have driven the Ordovician mass extinction event, as I explored in this earlier post.

Circulation and stratification

Sluggish ocean circulation used to be thought of as an important factor in anoxic events, but anoxia can occur even in actively circulating oceans. The reason is that upwelling of deep waters returns even more nutrients to the shallow ocean, enabling plankton to bloom, which as we saw above is the main driver of anoxia.

Past OAEs were long-lived affairs, so even though there may have been some thermal stratification of the surface ocean, which would have trapped nutrients and hindered the uptake of oxygen from the atmosphere, this would have been a transient effect, lasting a few centuries as compared to the OAE as a whole which typically lasted a few hundred thousand years. Stratification is a much more important factor in modern climate change.


Accidents of geography can create zones where nutrients are trapped, creating regions that are much more prone to anoxia than other areas. In the Cretaceous, for instance, the North Atlantic was much more restricted than it is now, and so was already prone to anoxia before OAE-2. During OAE-2, anoxic and euxinic waters expanded over a large portion of the oceans, depositing black muds rich in organic matter that are now oily black shales.

In the modern world, the Black Sea and the Gulf of Mexico, as well as some fjords, naturally trap nutrients making them prone to anoxia or euxinia. The Eastern Pacific is another area prone to low-oxygen because old, nutrient-rich waters well up along the coast, leading to large oxygen minimum zones and shoaling of low oxygen waters, causing die-offs and long term reduction in fish stocks.


Deoxygenation and ocean acidification are closely linked. If CO2 levels rise fast enough to decrease the carbonate levels in the ocean, ocean acidification is the result (ie it’s not just about a lowering pH). Low carbonate saturation makes it harder for plankton to make carbonate shells, so they tend to be smaller and thinner, and organisms that make heavier shells may die out. The net effect of this is to reduce the “ballast effect” – it reduces the rate that organic particles sink into the deep levels of the oceans. This traps more nutrients near the surface of the ocean, exacerbating anoxia.

Low oxygen zones are also naturally more acidic due to life respiring food and generating CO2, an effect known as “respiration-driven acidification,” so as low-oxygen waters expand they amplify ocean acidification in affected areas.

Acidification also has a number of biogeochemical effects that promote anoxia. It changes the ratio of carbon to nitrogen, which in turn increases the production of organic carbon, increasing the demand for oxygen. Acidification also enhances nitrogen fixation, which captures nitrogen and converts it into a nutrient, which boosts plankton levels further, increasing shallow-water oxygen demand.

Anammox and nitrous oxide

Ammonium waste is oxidized by microbes in low-oxygen environments via a chemical process known as “anammox,” consuming oxygen and generating nitrous oxide (N2O). As low-oxygen environments expand so may the production of nitrous oxide, which is mostly emitted to the atmosphere, where it is a minor greenhouse gas.

Our very own Ocean Anoxic Event

Today, deoxygenation from climate change is already exceeding natural variability in the southern Indian Ocean, parts of the eastern tropical Paci?c, and the Atlantic Ocean. Coastal dead zones have spread exponentially since the 1960s, becoming more intense as a result not just of rising ocean temperatures, but also due to excess nutrients in runoff from the land. Low-oxygen, low-carbonate, low pH waters now bathe seabed habitats along the west coast of the Americas and other places such as the Bay of Bengal. Oxygen minimum zones in tropical and sub-tropical oceans have expanded significantly in recent decades, compressing habitats for many fish, and expanding the habitat for low-oxygen-tolerant species such as the Humboldt Squid. 

Timeframe of climate-induced deoxygenation exceeding natural variability (Long et al 2016)

Timeframe when deoxygenation will exceed the natural variability. Blue shades indicate that the human deoxygenation signal is detectable around now, green shades show the spread of deoxygenation expected between now and around 2050 under a business-as-usual scenario. Gray areas have high natural variability, so will need a longer time for the human-caused effects to be formally distinguishable from natural variability. Blank areas are where the parameter used in the model (σθ=26.5 potential density surface) is at the ocean surface. Figure from Long et al (2016).

A significant component of modern deoxygenation is due to ocean stratification – the formation of a warm water ‘lid’ at the ocean surface that resists mixing into deep water. Stratification inhibits the movement of surface oxygen into deeper water, and it also promotes nutrient trapping near the surface.  On geological timescales stratification is transient, lasting only a few centuries, so was probably not an important factor in the much longer-lasting OAEs of Earth’s past.

As rainfall becomes more intense and erosive, as ice recedes, and as we clear forests and land cover, the supply of nutrients pouring into the oceans keeps promoting the expansion of low-oxygen zones. Warmer temperatures will keep weathering rates, and therefore nutrient supply to the oceans, higher for centuries. Add-in warming and acidification from rising CO2 levels, and we have the complete list of ingredients to bake our very own Ocean Anoxic Event.

Just as in the Cretaceous OAE-2, where preexisting oxygen minimum zones expanded with global warming, so the Eastern Pacific is expected to suffer the greatest impact on marine biodiversity in the coming decades. Human-caused ocean deoxygenation is expected to become widespread globally by the 2030s or 2040s, and increase substantially through the end of the century if we continue business-as-usual CO2 emissions.

On top of all that, though, there is the positive feedback by deoxygenation onto global warming by a shallower remineralization depth, greater nitrous oxide emissions, and weakening of the organic carbon pump.

Ocean deoxygenation is the 3rd but less-reported member of an evil climate change trinity, along with global warming and ocean acidification. It is not so much another shoe dropping out of our CO2 emissions as it is a large boot kicking ocean ecosystems, with significant knock-on impacts for hundreds of millions of people who depend on the oceans for a living, and with feedbacks on climate. Ocean scientists have been calling for policymakers’ urgent attention on this issue, and the Royal Society will be hosting a conference on the topic at The Royal Society in London in September 2016.

Main References:

Scripps Institution of Oceanography, Scripps O2 Global Oxygen Measurements (2016),

World Ocean Atlas 2013, Volume 3: Garcia, H. E., R. A. Locarnini, T. P. Boyer, J. I. Antonov, O.K. Baranova, M.M. Zweng, J.R. Reagan, D.R. Johnson, 2014. World Ocean Atlas 2013, Volume 3: Dissolved Oxygen, Apparent Oxygen Utilization, and Oxygen Saturation. S. Levitus, Ed., A. Mishonov Technical Ed.; NOAA Atlas NESDIS 75, 27 pp.

Bochdansky, A. B., Clouse, M. A., & Herndl, G. J. (2016). Dragon kings of the deep sea: marine particles deviate markedly from the common number-size spectrum. Scientific reports6.

Meyer, K. M., Ridgwell, A., & Payne, J. L. (2016). The influence of the biological pump on ocean chemistry: implications for long-term trends in marine redox chemistry, the global carbon cycle, and marine animal ecosystems. Geobiology.

Gehlen, M., Gruber, N., Gangstø, R., Bopp, L., & Oschlies, A. (2011). Biogeochemical consequences of ocean acidification and feedbacks to the earth system. Ocean acidification1, 230-248.

Kwon, E. Y., Primeau, F., & Sarmiento, J. L. (2009). The impact of remineralization depth on the air–sea carbon balance. Nature Geoscience,2(9), 630-635.

Marsay, C. M., Sanders, R. J., Henson, S. A., Pabortsava, K., Achterberg, E. P., & Lampitt, R. S. (2015). Attenuation of sinking particulate organic carbon flux through the mesopelagic ocean. Proceedings of the National Academy of Sciences112(4), 1089-1094.

Keeling, R. F., Körtzinger, A., & Gruber, N. (2010). Ocean deoxygenation in a warming world. Marine Science2.

Gilly, W. F., Beman, J. M., Litvin, S. Y., & Robison, B. H. (2013). Oceanographic and biological effects of shoaling of the oxygen minimum zone. Annual Review of Marine Science5, 393-420.

Wright, J. J., Konwar, K. M., & Hallam, S. J. (2012). Microbial ecology of expanding oxygen minimum zones. Nature Reviews Microbiology10(6), 381-394.

Monteiro, F. M., Pancost, R. D., Ridgwell, A., & Donnadieu, Y. (2012). Nutrients as the dominant control on the spread of anoxia and euxinia across the Cenomanian?Turonian oceanic anoxic event (OAE2): Model?data comparison. Paleoceanography27(4).

Danovaro, R., Molari, M., Corinaldesi, C., & Dell’Anno, A. (2016). Macroecological drivers of archaea and bacteria in benthic deep-sea ecosystems. Science Advances2(4), e1500961.

Moffitt, S. E., Moffitt, R. A., Sauthoff, W., Davis, C. V., Hewett, K., & Hill, T. M. (2015). Paleoceanographic insights on recent oxygen minimum zone expansion: Lessons for modern oceanography. PloS one10(1), e0115246.

Naafs, B. D. A., Castro, J. M., De Gea, G. A., Quijano, M. L., Schmidt, D. N., & Pancost, R. D. (2016). Gradual and sustained carbon dioxide release during Aptian Oceanic Anoxic Event 1a. Nature Geoscience.

Dupont, S., Todgham, A. E., Levin, L. A., Milke, L. M., Seibel, B. A., Cai, W. J., ... & Breitburg, D. L. (2015). And on top of all that…: Coping with ocean acidification in the midst of many stressors.

Melzner, F., Thomsen, J., Koeve, W., Oschlies, A., Gutowska, M. A., Bange, H. W., ... & Körtzinger, A. (2013). Future ocean acidification will be amplified by hypoxia in coastal habitats. Marine Biology160(8), 1875-1888.

Long, M. C., Deutsch, C., & Ito, T. (2016). Finding forced trends in oceanic oxygen. Global Biogeochemical Cycles30(2), 381-397.

Diaz, R. J., & Rosenberg, R. (2008). Spreading dead zones and consequences for marine ecosystems. science321(5891), 926-929.

Capone, D. G., & Hutchins, D. A. (2013). Microbial biogeochemistry of coastal upwelling regimes in a changing ocean. Nature Geoscience6(9), 711-717.

Levin, L. A., & Breitburg, D. L. (2015). Linking coasts and seas to address ocean deoxygenation. Nature Climate Change5(5), 401-403.

Levin, L. A., & Le Bris, N. (2015). The deep ocean under climate change. Science350(6262), 766-768.

Segura, C., Sun, G., McNulty, S., & Zhang, Y. (2014). Potential impacts of climate change on soil erosion vulnerability across the conterminous United States. Journal of Soil and Water Conservation69(2), 171-181.

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Comments 1 to 8:

  1. Very nice presentation.One of the best summaries I have seen.

    Important point to make is that the expanded anoxic zone is a transient, because the ocean is heated from the top but mixed by winds and tides. The density gradient across the thermocline strengthens as global temperatures go up, making it more difficult to mix water and oxygen down. 

    Eventually as the ocean warms and the gradient drops, there will be more exchange. However, warm temperatures still cause organic matter degradation shallow and maintain higher atmospheric CO2.

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  2. Interesting summary Howard.

    Do you think the remineralization depth changes during ice ages may explin the phenomenon of strong CO2 feedback of the initial orbital forcings?

    Oceanographers have been saying that the CO2 feedback responsible for the magnification of orbital forcings comes from the ocean degassing. But they don't know or are unsure of the mechanism responsible for such degassing and regassing cycles that dominated climate cycles of the last 1My.

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  3. Mitch - in talking to people who know way more about this than I do, they tell me that the thermal stratification is indeed transient exactly as you describe, but anoxic conditions in Ocean Anoxic Events sometimes lasted hundreds of millennia, well beyond the shelf-life of stratification, suggesting a prolonged enhanced nutrient supply, which seems to be linked to enhanced weathering rates in a warmer, wetter climate. 

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  4. Thanks Howardlee,
    Sobering indeed, also interesting how recent CO2ppm 12 month apart month on month rises are increasing whilst emissions are apparently falling, is there evidence that this natural positive feedback or others (forest fires) are possibly already starting in earnest?
    What do think iron fertilization will do to the fine balance of things?
    Do you think sea level rises invading nutrient rich lands and soils will have any significant affect?
    And lastly sorry for so many questions, what are your thoughts on how the increase in runoff nutrients caused by the expansion of industrial farming may affect things?
    Does seem more and more that a huge carbon sequestration effort is going to be needed and keeping the oceans healthy and carbon sequestering through the warming coming is going to be a vital challenge.
    Mind you if over activates like over fishing, waste, pollutants, etc, somehow just stopped occurring then maybe the surface oceans might actually get healthier for while despite the accelerating warming period being experienced.

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  5. Chriskoz - I believe that remineralization effects were accounted for in carbon pump calculations which explain some but not all of the 80-100ppm CO2 drawdown in glacial times. As Prof Archer noted in his book The Global Carbon Cycle (2010) "There is no single satisfactory explanation for the positive ocean carbon cycle feedback responsible for the glacial and interglacial atmospeheric CO2 cycles."

    I brought this up in my interview with Prof Andy Ridgwell last December, and he said:

    "I suspect it’s more likely we have all the mechanisms known but it’s how we piece the whole thing together consistent with all the different bits of proxy information we have. Now that the CO2 record of the glaciation is getting better and better resolved in time, they are looking like 100-year steps of 20 - 25 ppm CO2 and there’s some radiocarbon evidence that this carbon must have been mostly radiocarbon-dead. So people have been thinking: could it have been rapid sea rises? Could it have been destabilizing permafrost or marine hydrates? In terms of really trying to interrogate the highest resolution ice core record of the glaciation and actually see within a general change in the carbon cycle between glacial and interglacial, are there particular mechanisms that might be giving a huge kick of CO2 at certain times? If you just flood permafrost with ocean that’s not at freezing temperature, then you suddenly melt the permafrost so you can have a lot of carbon release just because the sea level rise is massive."

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  6. Ranyl - I'll answer in sequence:

    Remineralization depth CO2 feedback starting in ernest?
    I don't know, but it's a plausible factor among many including fires that you mention. The Global Carbon Budget shows that the ocean carbon sink continues to increase at about 10 GtCO2/yr but there is large yearly variation in those data. Kwon et al said: "...considerable fractions (more than 30%) of the full response occur on timescales of decades..." and: "... changes in remineralization depth could feed back on twenty-first century climate change." And "... our work suggests that the impact on the global carbon cycle could be substantial."

    Iron fertilization:
    Iron fertilization is nutrient supply, so it would tend to increase anoxia, provided other essential nutrients like phosphorus, nitrogen, etc are present in the Redfield Ratio.

    Inundation of nutrient-rich land:
    Yes this should increase nutrient supply at least in coastal areas.

    Industrial farming:
    Yes this is one of the major factors behind the exponential increase in coastal dead zones since the 1960s.

    Carbon sequestration: Yes. See Andy Skuce's excellent 3-part article on "The Road to 2 degrees"

    The bottom line is that the climate system is complex machinary that we've stuck multiple fingers into. All the knock-ons and feedbacks - positive and negative - are highly tangled. But evidence from Earth's past show that the positive feedbacks exceed the negative ones on a human timeframe, before he negative ones win out on a geolgical timeframe of many millennia.


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  7. Thanks Howard...

    Road to 2C is inevitable I suspect now even with negative emissions.

    Early Pliocene 3-5C hotter with a max CO2 400ppm and average more like 350ppm from many recent papers and were at 480ppmCO2e.

    Its going to take a huge brake to stop this rollcoaster ride.

    However we have depleted almost every ecosystem and therefore their regenration might bring CO2 in check to some degree.

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  8. A really thought provoking article here and thanks for that Howard. Not only is exceesive nutients caused naturally by a warming world with more precipitation but due to the Haber process we are at the same time considerably adding to this excess. 

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