In a paper in Science in 1977, David Schindler showed, using whole-lake experiments, that natural biological mechanisms can compensate for deficiencies in carbon and nitrogen in lakes affected by eutrophication, but no such mechanisms exist for phosphorous. Based on his findings, Schindler recommended that management of lakes should focus on control of phosphorous levels. Forty years after the paper was published, I asked David Schindler about his motivation to do this experiment, its impact on lake management and what we have learnt about this topic since then.
Citation: Schindler, D. W. (1977). Evolution of phosphorus limitation in lakes. Science, 195(4275), 260-262.
Date of interview: Questions sent by email on 27th November 2016; responses received by email on 17th January 2017.
Hari Sridhar: I would like to start by asking you about the motivation for this paper. From looking at your profile online I learnt that this paper came approximately 10 years after you started working on the Experimental Lakes Area project. Could you tell us a little about the origins of this paper and the work presented in it?
David Schindler: Our very first experiment was begun in 1969, to test the claim of the soap and detergent companies that carbon, and not phosphorus, was the nutrient limiting eutrophication, and that the proposed regulation of phosphorus in the Great Lakes by the International Joint Commission would be a waste of money.
In 1968, our first year, we did surveys of over 50 small lakes, and found that lake 227 had the lowest carbon content ever recorded. We decided that an extreme test of the carbon theory would be to add P and N but no C. If this oligotrophic lake became eutrophic it would destroy the carbon theory. That is what happened (Schindler et al. Science 1972) and the carbon theory was abandoned. Our measurements showed that the carbon was drawn from the atmosphere, to replace that used as photosynthesizing algae used the CO2 in the lake. Thus, the carbon cycle could slowly adapt to keep carbon proportional to the phosphorus supply.
In a second experiment, in the double-basin Lake 226, we added nitrogen and carbon to both basins, but phosphorus only to one basin. The latter basin became eutrophic. In contrast to Lake 227, where increases in several of the naturally-occurring species had accounted for the increase in algae, in Lake 226, it was a few species of nitrogen-fixing cyanobacteria that responded. The major difference that I hypothesized could have caused this difference in response was the N:P ratio. In Lake 227, it was greater than the relative N:P in algae (the so-called Redfield Ratio). In Lake 226, the N:P supplied had less N than required to balance the P in algal structure, similar to the ratio in sewage. It occurred to me that perhaps Lake 226 was reacting like Lake 227, except drawing N from the atmosphere. The difference would be that while all algal species are capable of fixing C, only a few species of diazotrophic cyanobacteria can fix N as a gas, thus they were favored by low N. To further test this hypothesis, we cut the N fertilizer in Lake 227, while keeping P fertilizer the same. The lake responded the same as Lake 226. Then in looking at all of the experiments we had done in whole lake, it was clear that it did not matter how much N or C was added as fertilizer. Biogeochemical mechanisms were capable of keeping the two elements closely in balance with phosphorus. So the key was to control phosphorus. That was the basis for this paper, and subsequent experiments and phosphorus control case-histories have shown that it was correct. The paper is as relevant today as it was in 1977.
HS: Stepping back a bit, could you tell us how you got interested in this area of research? Again, from looking at your publication profile, I came to know that your work on lake ecosystems started as early as your PhD. When did this interest start?
DS: My interest in lakes started as a child. I grew up in northern Minnesota’s lake country, and got to lakes whenever I could, to fish, swim, watch birds. Then as an undergraduate, I got a summer job in aquatic research that resulted in two research papers. I learned that I could turn my passion into a career. By the time I was a second year undergraduate, I had decided that I would get a PhD and become a research scientist.
HS: Could you give us a sense of how these whole-lake experiments were actually done, i.e. how many people were involved, what was your daily routine like when you were doing them, how difficult was the work etc.?
DS: This varied a lot with the lake’s size, location, and what was done to the lake. Often it meant stockpiling several tonnes of chemicals on the lake’s shore. There were no roads to them, so this was done in winter, when ice and snow made it possible to haul sleds pulled by snow machines, or to use a helicopter and land chemicals on the ice to be carried to shore and cached for summer use. While in progress, usually a team of two people did all of the taking of routine samples for chemistry and plankton analysis and physical parameters, and also made the chemical additions. Once samples were in hand they were preserved and sent to specialists in plankton identification and counting. We did perishable chemical analysis at a lab at the main camp site, about 30 minutes travel from the most remote lakes. Less perishable analyses were sent to the main chemical lab in Winnipeg, at the Freshwater Institute. Overall, about a dozen people were involved, but they did the work for several different experiments.
HS: Do you remember how long it took you to write the paper, and when and where you did most of the writing?
DS: I always did most of the writing in the ELA field camp. I would rise at sunrise, write for a few hours, then have breakfast. Once written, I sent it to a few colleagues to critique. My mind was always clear in the morning, and it only took a couple of days.
HS: How did you draw the figures for this paper?
DS: I plotted them first by hand on ordinary graph paper. My technician, Therese Rusczynzki, helped with calculations and final plotting. Then they were sent to the Freshwater Institute drafting department for final figures of a quality good enough for a journal. Today all of this could be done in a couple of hours on a laptop.
HS: If you don’t mind, I would like to go over the names of people you acknowledge to find out a little more about who they were, how you knew them and how they helped:
Ruzczynski: see my comment above.
Mike Stainton and Jim Prokopowich: did the perishable chemical analyses.
Kaz Patalas: critiqued my draft manuscript.
Robert Flett: confirmed that the cyanobacteria blooms were indeed fixing nitrogen, using acetylene reduction methods.
Ron Reid, Russ Schmidt and a number of undergraduate summer helpers: took samples every week or two from all of the lakes.
Everett Fee: critiqued my draft manuscript
HS: Do you continue to work in the Experimental Lakes Area? When was the last time you visited these lakes? Could you give us a sense of how these lakes have changed since the time you did this study?
DS: I continue to work with the data set, and collaborate with scientists there, although I now live in British Columbia and have not been there for 15 years. The lakes haven’t changed much, as it is still a remote area, with few people. The nearest community is about 50 km distant. Some of the catchments burned, thanks to forest fires in 1974 and 1980. But these again look like middle-aged forests today.
HS: Did this paper have a relatively smooth ride through peer-review? Was Science the first place you submitted this to?
DS: It was accepted almost without change. My mind works like the Science papers of the day, bold statements, with the caveats and discussion in a large footnote section. I liked it better than the current form of the journal.
HS: Do you remember how this paper was received when it was published? Did it attract a lot of attention and discussion?
DS: It did. The paper led directly to the modifications to the Great Lakes Quality Agreement in 1978 that have resulted in a very successful recovery of the lakes, by controlling phosphorus. Sadly, they did not control non-point sources of phosphorus in the policies of the day, and intensifying land use threatens to bring the problem back as phosphorus is still not controlled well enough from agriculture.
HS: This paper has been cited over 2000 times. At the time you did the study did you have any inkling how important it would turn out to be? Do you have a sense of what the paper mostly gets cited for?
DS: It would have been cited much more if there had been methods to track citations back then. I think that it is fair to say that this paper and its 1974 companion (also in Science) are widely regarded as the start of the phosphorus control policy shift.
HS: Did this paper have any kind of direct impact on your career? In what way did it influence the future course of your research?
DS: It probably did, but no more than my 1972 and 1974 papers in Science, or several more on acid rain experiments. The Canadian Department of Fisheries always did, and continues to downplay the work of its scientists. It would have gotten more attention if I had been at a university.
HS: Today, nearly 40 years after it was published, would you say the main conclusions still hold true, more-or-less?
DS: Yes. We have repeatedly tested the main conclusions, and they are very solid (see my 2008, 2012, and 2016 papers). Now there are many well-documented case history studies of large lakes that show the generality of our findings.
HS: If you were to redo these experiments today, would you change anything about them?
DS: Of course, more modern methods would allow us to do a better job, but there is not much else I would change.
HS: At one point in the paper you say “At this time I cannot explain why different genera of nitrogen fixers should be dominant in the two lakes. The difference may be due to differences in other micro-nutrients or growth inhibitors and requires further investigation.”
Did such investigations happen subsequent to this paper?
DS: Algal physiologists have spent years trying to deduce the chemical nuances and competitive interactions that allow different species to thrive in different conditions, and we still do not understand them. I believe that at low N:P input, it can safely be predicted that nitrogen fixers will outcompete species that cannot use atmospheric sources, but we still cannot predict which of several species of nitrogen fixers will dominate.
HS: In the Discussion you say “I hypothesize that only lakes which have experienced very recent increases in the phosphorous input, without corresponding increases in nitrogen and carbon, or those receiving enormous influxes of phosphorous will not show the correlation between total phosphorous and standing crop.”
Were these hypotheses tested and supported by subsequent research?
DS: Our subsequent work has shown that the nitrogen and carbon cycles can take years to catch up if phosphorus input is increased. So the response of algal standing crop is not rapid, unless a lake is also supplied with all the nitrogen, carbon, and other elements that algae need. As a result, it is folly to predict what will happen when phosphorus is decreased from small-scale experiments where phosphorus is added. Yet, this is exactly what most limnologists continue to do.
HS: You say “The “evolution” of appropriate nutrient ratios in freshwaters involves a series of interrelated biological, geological, and physical processes, including photosynthesis, the selection of species of algae that can utilize atmospheric nitrogen, alkalinity, nutrient supplies and concentrations, rates of water renewal and turbulence. It is impossible to visualize a laboratory experiment that could realistically represent all of these parameters.”
DS: It is impossible. It would involve realistically simulating geological, physical and weather conditions, and maintaining these for years in a laboratory setting. Better to do a few experiments, then build a data base of case histories to flesh out details.
HS: Today, could you reflect on this statement and tell us whether on this remains the same or has changed in any way?
DS: I would not change a word.
HS: At the end of your paper, based on your experiments, you make some recommendations for management of lakes, including that decisions should be based on field tests and lab bioassays. Could you reflect on how much of an impact this study has actually had on lake management?
DS: I think the impact has been slow. It has gathered momentum as many case-histories of lakes where phosphorus has been controlled accumulate in the literature, as shown in our 2016 paper in Env. Sci. and Technol. But there are dozens of ambitious young scientists always probing for flaws in the arguments, and this continues. But alternative theories have no successes to back up their claims, so the case for P control gains momentum.
HS: In the 40 years since this paper was published, have you ever read it again? If yes, in what context? Wat strikes you most about it when you read it now?
DS: What strikes me about it is how flawless the arguments were, considering my limited experience. Mother Nature is an excellent teacher, especially when compared to papers and textbooks.
HS: Would you count this as one of your favourites, among all the papers you have published?
HS: What would you say to a student who is about to read this 40-year old paper today? What should he or she take away from it? Would you add any caveats?
DS: My main caveat to students is to read carefully and think about the arguments presented. Most papers published today are riddled with spurious arguments that students accept as fact. Spend more time in the field than reading, and when there, maintain an open mind. Much of what is written is simply false.