[Coral-List] unprecedented fixed nitrogen

[Charles Birkeland]

The Coral-List communications on “What can scientists do?” about human-caused global changes affecting corals have focused entirely on CO2 buildup and the resulting increased global warming, decreased aragonite saturation levels (lower pH of seawater), and rising sea level. Of course the increased CO2 is a very serious problem, but scleractinian corals have survived this stress several times in the past while the sudden global buildup of fixed nitrogen is probably unprecedented. Further, changes in the physical environment such as CO2 buildup over geological time have been aimlessly up and down while the buildup of fixed nitrogen may cause a progressive arms race in both ecology and evolution in directions that favor algae and heterotrophs to the detriment of symbiotic photosynthetic holobionts.

Scleractinians have been around for over 220 million years, but for long periods during this time, the CO2 was at high levels in the atmosphere and the aragonite saturation levels were low. Coral reefs were prevalent in the mid Mesozoic, but from the later Jurassic and throughout the Cretaceous, while the hermatypic scleractinian corals increased in diversity, the development of coral reefs became less prevalent (Hallock 1997). The global warming, the decreased aragonite saturation levels, and extreme sea level rise in the later Mesozoic were probably resulting from abundant CO2 output by extensive submarine volcanism with the relatively rapid rifting and movements of continental plates (Hallock 1997). The finishing blow came with the CO2 from the Deccan Traps continental volcanic mantle plume 500,000 km2 in area and > 2,000 m thick. The atmosphere in the Upper Cretaceous is estimated to have had 4 times the concentration of CO2 as in the atmosphere today. The sea level rose
 to over 200 m higher than it is today and only 18 to 20 % of the surface of Earth was above seawater. Polar waters were generally warmer than 20 °C during the middle Cretaceous (Jenkyns et al. 2004). As the saturation level of aragonite decreased, the scleractinian reefs gave way to reefs of rudist bivalves, whose shells were predominantly calcite.

Scleractinian reefs disappeared from the geological record well before the end of the Cretaceous (Copper 1994), remained absent throughout the Paleocene, and did not reappear until the Eocene. Although coral reefs were gone for over 10 million years, fossils indicate that Heliopora, Stephanocoenia, Madracis, Astreopora, Goniopora, Porites, Siderastrea, Cycloseris, Oculina, Dichocoenia, Hydnophora, Cladocora, Diploastrea, Diploria, Favia, Leptoria, Heteropsammia and others had survived during  this long absence of coral reefs (Wells 1956, Veron and Kelly 1988, Paulay 1997).

Kleypas et al. (2001) suggest that times favorable for reef growth have been only 10% of the past few million years. The past few centuries that we humans have experienced were abnormally favorable for reef growth. “Like obesity, a massive reef accumulation may be the result of remaining stationary too long under good conditions” (Buddemeier and Kinzie 1998). But whether or not the corals are in danger of extinction, humans will suffer when reef growth ceases or slows. With sea level rising at the same time as the pH of surface waters decreases, reefs are likely to drown and as sea level rises, reefs will not provide protection of coastal areas against storm waves and shoreline erosion, nor the habitat and topographic complexity that provides abundant fisheries stocks. 

Since corals have a heritage of extreme fluctuations in atmospheric CO2, they might have inherited the capacity to survive this next coming round. In contrast, the doubling of fixed nitrogen on Earth in the past few decades by use of fossil fuels (Vitousek et al. 1997) is unprecedented. The production of CO2 is generally an easy downhill byproduct of the burning of materials created by photosynthesis, whether by metabolism of biota or through the use of fossil fuels. The ups and downs of global atmospheric CO2 because of volcanism and use of photosynthetic products are natural. But nitrogen fixation by combination of nitrogen with hydrogen, oxygen, or carbon is an expensive energy-consuming uphill process. Our industrial production of food is replacing agricultural production by subsidizing traditional solar energy with the use of fossil fuels to produce fertilizers by fixing nitrogen (Pollan 2006). By using fossil fuels, we are compounding the climate-change problem by addi
ng more CO2 as well as N2O to provide the greenhouse effect as we produce fertilizer. Nitrous oxide has 296 times more influence on global warming than the same per mass unit of carbon dioxide.

Fritz Haber was awarded the Nobel Prize in 1920 for inventing the method of using fossil fuels to fix nitrogen because this procedure was “the most important invention of the 20th century” (Pollan 2006). Carl Bosch estimated that two of every five humans on Earth would not exist at this time if not for this invention. Mainland China constructed thirteen massive fertilizer factories which are considered to have prevented starvation. But with a subsidy from fossil fuels, high yield became the driving force and “time is money, and yield is everything” (Pollan 2006). With subsidies, efficiency and frugal use of resources means little. “Every bushel of industrial corn requires the equivalent of between and quarter and a third of a gallon of oil to grow it” and the federal treasury now spends up to $5 billion a year subsidizing cheap corn (Pollan 2006). With fossil fuel subsidy, the farmers do not need to risk erring on the side of too little fertilizer, and so they waste much of 
the fertilizer they buy by providing far more than is needed. This excess of nitrates and phosphates drain into the rivers. In the 1990s, the Mississippi carried 10 times the nitrates and phosphates that it did in the 1960s (Hallock et al. 1993). The load might be substantially more these days. 

By fertilizing algae (phytoplankton), the excess fertilizer has created at least 146 large-scale dead zones in coastal oceans of the world in which fishes and crustaceans and other animals suffocate from oxygen depletion.  The dead zone south of Louisiana, fertilized by the Mississippi, occasionally gets to be as large as the area of Massachusetts. The identity of the limiting nutrient is a complicated story, but whether it is N, P, Fe, Si, C or others, these large-scale dead zones are associated with fertilizers from industrial nitrogen-fixation.

With surplus nutrients, time and yield are everything, and survival in competition for space by efficiency with recycling loses in a major way.  This is especially true for coral reefs. Coral holobionts are excellent at living in oligotrophic situations because of efficiency and recycling, but surplus nutrients from upwelling and runoff favor profligate growth and biomass accumulation, both to the detriment of the individual coral recruit (Birkeland 1977) and at the level of geographic patterns of community structure and ecosystem processes of coral reefs (Birkeland 1988, 1997). Geerat Vermeij (1995) perceives surplus nutrients as favoring major evolutionary innovations. John Taylor also (1997) discusses evolutionary implications of different regimes of nutrient input. Under conditions of surplus nutrients, profligate yield would favor rapid growth of algae and heterotrophic benthic animals over efficient recycling of nutrients by autotrophic holobionts.

So why is this of interest? This pattern might provide insight into why the reefs of American Samoa are so resilient compared to those in the tropical western Atlantic. The corals on American Samoa have been subjected to overfishing of herbivorous fishes (Page 1998, Craig and Green 2005), scarcity of urchins (Birkeland 1989), hurricanes, bleaching, crown-of-thorns outbreaks, pollution, sediment, yet they continually rebound with vigor (Birkeland et al. 2008). Crustose coralline algae are prevalent and macroalgae are not. Sponges such as Dysidea herbacea that host photosynthetic symbionts are prevalent and dominate large areas of reef, while heterotrophic Stylotella sp. are scarce and diminutive. Likewise, the colonial tunicate Diplosoma similis, with photosynthetic symbionts, covers large areas at the bases of corals, while the heterotrophic tunicates are scarce. American Samoan reefs possibly have resilience partially because they are distant from the massive fixed nitrogen
 and fertilizer runoff of continental areas, whereas nearly all of the Caribbean is close to continents. A respectable diversity of coral disease can be found in American Samoa (Work and Rameyer 2002), but they have not been found to take over the corals as they have in the Caribbean (Aronson and Precht 2001). Experiments by Bruno et al. (2003) suggest a hypothesis that input of fixed nitrogen in the western Atlantic in recent decades might contribute to the vulnerability of corals. 

In response to the question “What can scientists do?”, we should educate or warn the public that subsidizing production in unnatural ways can be unsustainable and will possibly lead to system collapse and to future conflict. The government subsidies for use of fossil fuels to increase industrial food production (Pollan 2006) and for harvesting fisheries resources when the reproductive stock is too low to sustain the fishery (Iudicello et al. 1999) do not take into account the future consequences. We may be building a human population beyond carrying capacity, subsidized by finite fossil fuels rather than by practically infinite solar radiation alone. Agricultural food production was based on efficiency and free nitrogen fixation by alternating corn production which depleted nitrogen from the soil with soy bean, alfalfa, or other legume production which fixed nitrogen “for free” (by infinite solar radiation). Industrial food production bypassed this slow process by pouring fo
ssil fuel into the process, thereby encouraging profligate application of fixed nitrogen into the system, and eventually unprecedented input into marine environments. This global fossil fuel subsidy of production of fixed nitrogen is favorable to the traits of algae and heterotrophic organisms, and not corals.

Aronson, R.B., and W.F. Precht. 2001. White-band disease and the changing face of 
	Caribbean coral reefs. Hydrobiologia 460: 25-38

Birkeland, C. 1977. The importance of rate of biomass accumulation in early 
	successional stages of benthic communities to the survival of coral recruits. Proc. 
	3rd International Coral Reef Symp., Miami 1. Biology: 15 - 21

Birkeland, C. 1988. Geographic comparisons of coral-reef community processes. Proc. 6th Internat. Coral Reef Symp., Townsville 1:211-220

Birkeland, C. 1989 The influence of echinoderms on coral-reef communities. Pages 1-79 In M. Jangoux and J.M. Lawrence (eds.), Echinoderm Studies 3. Balkema, Rotterdam

Birkeland, C. 1997. Geographic differences in ecological processes on coral reefs. Pages 273 to287 In C. Birkeland (ed.), life and death of coral reefs. Chapman & Hall, NY

Birkeland, C., P. Craig, D. Fenner, L. Smith, W.E. Keine, and B. Riegl. 2008. Geologic 
	setting and ecological 	functioning of coral reefs in American Samoa. Pages 737 – 	761 In B. Riegl and R.E. Dodge (eds.) Coral Reefs of the USA. Springer, NY 

Bruno, J.F., L.E. Petes, C.D. Harvell, and A. Hettinger. 2003. Nutrient enrichment can 
	increase the severity of coral diseases. Ecology Letters 6: 1056-1061

Buddemeier, R.W., and R.A. Kinzie III. 1998. Reef science: asking all the wrong 
	questions in all the wrong places? Reef Encounter 23: 29-34

Copper, P. 1994. Ancient reef ecosystem expansion and collapse. Coral Reefs 13:3-11

Craig, P., and A. Green. 2005. Overfished coral reefs in American Samoa: no quick fix. 
	Reef encounter 33: 21-22

Hallock, P. 1997. Reefs and reef limestones in Earth history. Pages 13 – 42 In C. 
	Birkeland (ed.), Life and death of coral reefs. Chapman & Hall, NY

Hallock, P., F.E. Müller-Karger, and J.C. Hallas. 1993. Coral reef decline. Natl. Geogr. 
	Res. Explor. 9: 358-378

Iudicello, S., M. Weber, and R. Wieland. 1999. Fish, markets, and fishermen: the 
	economics of overfishing. Island Press, Washington, DC. 192 p.

Jenkyns, H.C., A. Forster, S. Schouten, and J.S. Sinninghe Damsté. 2004. High 
	temperatures in the late Cretaceous Arctic Ocean. Nature 432: 888-892

Kleypas, J.A., R.W. Buddemeier, and J.-P. Gattuso. 2001. The future of coral reefs in an 
	age of global change. Int. J. Earth Sciences 90: 426-437

Page, M. 1998. The biology, community structure, growth and artisanal catch of 
	parrotfishes of American Samoa. Report to the Department of Marine and 
	Wildlife Resources, Government of American Samoa. 78 p.

Paulay, G. 1997. Diversity and distribution of reef organisms. Pages 298 – 353 In C. 
	Birkeland (ed.), Life and death of coral reefs. Chapman & Hall, NY 

Pollan, M. 2006. Omnivore’s dilemma. Penguin Books, London

Taylor, J.D. 1997. Diversity and structure of tropical Indo-Pacific benthic communities: 
	relation to regimes of nutrient input. Pages 178-200 In R.F.G. Ormond, J.D. Gage, 
	and M.V. Angel (eds.), Marine diversity:patterns and processes. Cambridge Univ. 
	Press, Cambridge

Vermeij, G.J. 1995. Economics, volcanoes, and Phanerozoic revolutions. Paleobiology 
	21: 125-152

Veron, J.E.N., and R. Kelly. 1988. Species stability in reef corals of papua New Guinea 
	and the Indo-Pacific. Australasian Assoc. Paleontol. Mem. 6: 1 – 69

Vitousek, P.M., H.A. Mooney, J. Lubchenco, J.M. Melillo. 1997. Human domination of 
	Earth’s ecosystems. Science 277: 494-499

Wells, J.W. 1956. Scleractinia. Pages F328-F444 In R.C. Moore (ed.), Treatise on 
	invertebrate paleontology, Part F, Coelenterata. Univ. Kansas Press, Kansas City

Work, T.M., and R.A. Rameyer. 2002. American Samoa reef health survey. Report to US 
	Fish and Wildlife Service by the USGS National Wildlife Health Center, Hawaii 
	Field Station, Honolulu, Hawaii. 41 p.