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Parrotfish, Nutrients, and Control of Algae

A recent paper published in Nature uses a mathematical model of coral cover, macroalgae cover, turf algae cover, and grazing by parrotfish and concludes that only parrotfish grazing can prevent algae from overgrowing and killing corals. It blames fishermen for catching parrotfish and causing algae growth, and makes the policy recommendation that fishermen should be stopped in order to let the corals recover. These conclusions have been widely covered in the press.

However close examination of the model reveals that these conclusions are no more than a restatement of the original assumptions built into the model. As a someone with experience doing mathematical modeling in astronomy, spatial population distributions, biogeochemistry, atmospheric chemistry, and paleoclimatology, I am acutely aware that no model is better than its assumptions, and if these don't adequately describe reality, the results are simply intellectual artifacts rather than providing insight into how nature works. If we misunderstand the key controlling factors, the management prescriptions we make cannot possibly work.
 
The model published in Nature allows corals to die only by being overgrown by algae, and by "natural" coral mortality, which is equated with hurricane destruction, that is to say, it does not include mortality from heat shock or new diseases, the major causes of coral mortality in most places in the last few decades. The model specifies that algae grow at a constant rate, and can only die by being grazed. There is no allowance for algae fragmentation by waves (anyone diving after a storm knows the bottom can be covered with algae ripped loose), nor is there any allowance for intrinsic factors that may vary the rate of algae growth. Now it is long known that benthic algae growth can vary by orders of magnitude depending on nutrient concentrations, but nutrients nowhere figure in the model as a factor affecting algae growth. Hence the model's conclusion that only grazing can limit algae growth, as was assumed in the first place. This tautology somehow escaped the peer reviewers.
 
The model predicts that the more parrotfish the less algae, but anyone who has actually watched the long term changes in algae and parrotfish knows that as algae populations increase, so do the numbers of parrotfish. The model uses the misnamed "phase shift" interpretation of the long term changes in algae, corals, and fish in Jamaica that attributes algae abundance to Diadema die off and overfishing, and which blames the fishermen for eating all the herbivorous fish. But in fact, long term observations of changes in reefs all around Jamaica show that algae overgrowth took place at different times in different places over a 40 year period, and every place they followed local population growth and sewage inputs to coastal waters, but did not follow overfishing or Diadema mortality except coincidentally at a few places, such as Discovery Bay that went eutrophic at the same time (T. J. Goreau, 1992, Bleaching and reef community change in Jamaica: 1951-1991, SYMPOSIUM ON LONG TERM DYNAMICS OF CORAL REEFS, AMERICAN ZOOLOGIST, 32: 683-695), and that algae growth was strongly linked to excessive nutrients from land based sources (T. J. Goreau & K. Thacker, 1994, Coral Reefs, sewage, and water quality standards, PROC. 3D. CARIBBEAN WATER AND WASTEWATER ASSOCIATION CONFERENCE, WATER AND WASTEWATER NEEDS FOR THE CARIBBEAN: 21ST CENTURY, Kingston, Jamaica, 3:98-116 and many papers by Brian Lapointe). In fact in this period Jamaican fish populations changed from being dominated by fish and invertebrate eating species to near complete dominance by herbivores, the exact opposite of what the hypothesis of top-down control of algae by herbivores, like this recent model, predicts, but fully consistent with the bottom-up hypothesis that algae productivity, and herbivore populations, are controlled by nutrient inputs.
 
The practical management question is: how can weedy algae be controlled before they smother coral reefs? To my knowledge there are only two published cases of weedy algae being removed from coral reefs on a large scale, one of them a short term success but a long term failure, while the other has been sustained.
 
In Kaneohe Bay, Oahu, Hawaii, sewage was pumped onto the reef, algae spread out from the sewage outfall and overwhelmed the reef, and since there was no doubt that the nutrients had caused the algae, a long sewage outfall was built to place the problem much further away. As the nutrients fell the algae died back, and the coral gradually recovered. After the point source of nutrients was removed, the suburbanization of the watershed caused uncontrollable increases in non-point sources of nutrients from lawn fertilizers, golf courses, road runoff, and other nutrients that were not flushed down the sewer. These have caused the system to again go eutrophic, and the algae have again smothered the reef. There is a large Hawaiian literature on this that is readily available. It shows that controlling nutrients gets rid of algae, but only if it is sustained.
 
A more successful long term case is a bay in Jamaica that I got cleaned up 10 years ago by diverting all the land based sources of nutrients and recycling them on land. Within weeks the red and green weedy algae smothering the reef began to die back, and two months later they were gone (T. Goreau, 2003, Waste Nutrients: Impacts on coastal coral reefs and fisheries, and abatement via land recycling, 28p., UNITED NATIONS EXPERT MEETING ON WASTE MANAGEMENT IN SMALL ISLAND DEVELOPING STATES, Havana, Cuba). I have just revisited this site 10 years after, and the weedy algae are still gone, with the algae now dominated by the oligotrophic calcareous algae.
 
In my experience the only way to get rid of weedy algae is to starve them of nutrients, and then they very quickly die. But all excessive nutrients must be controlled, and they must remain controlled. This requires adherence to the coral reef specific nutrient standards proposed by Brian Lapointe, Mark and Diane Littler, and Peter Bell. We can blame the victims by stopping fishermen from eating, but this will not work because it is based on a seriously flawed understanding of what controls algae growth.
 
The Turks and Caicos Islands are the first place in the world to propose coral reef specific water quality standards, and the only place in the world to require that all developers build sewage treatment plants and recycle all of their waste water on their own property. We will not see the algae die back in eutrophic reefs until other countries follow their example and all the sources of anthropogenic nutrients are identified and controlled.