In a paper published in Nature in 2003, Anne Magurran and Peter Henderson used a long-term dataset on estuarine fish to throw light on a puzzling pattern – a greater number of rare species than predicted by theory in large community assemblages. Magurran and Henderson showed this paradox can be explained by separating the dataset into two components – abundant species typical of the habitat being considered show the expected log normal pattern while rare species that have different habitat requirements show a log series distribution. Thirteen years after the paper was published, I spoke to Anne Magurran about how she became interested in this topic, her collaboration with Peter Henderson and what we have learnt since about species abundance distributions.
Citation: Magurran, A. E., & Henderson, P. A. (2003). Explaining the excess of rare species in natural species abundance distributions. Nature, 422(6933), 714-716.
Date of interview: 6th October 2016 (via Skype)
Hari Sridhar: What was the specific motivation for doing the work presented in this paper? I realize that, at this time, you’d already done quite a bit of work on biodiversity, including writing some books on the topic. What was the motivation for this particular piece of work?
Anne Magurran: The motivation was that I’d started to collaborate with my colleague, Peter Henderson. Peter had been incredibly insightful in collecting data from the Bristol Channel in southern England. The data were collected from an intake of a power station where Peter had been undertaking environmental monitoring since the early 1980s. Because samples were collected at the same phase of the tidal cycle every month, the water volume intake is the same, making a very consistent sample. At that time of our paper, sampling had occurred for 21 years; now the time series is over 30 years. It’s a wonderful case study for asking how biodiversity changes through time. As we began to explore the data set, we noticed that there were very strong differences between different classes of species. Some were very abundant – very persistent – and some were infrequent and also uncommon. And that explanation of the data he had collected was motivation for the paper.
HS: Could you tell us a little more about how the collaboration started? Did you get together to analyze this particular data set?
AM: I’ve known Peter for a long time. Before I came to St. Andrews, I was in Oxford University, and Peter was associated with the university. So I got to know him then. And I’ve also worked in the Amazon with Peter. Peter was involved in the very early days in setting up Mamirauá Sustainable Development Reserve, and through him I got to visit the Amazon as well. So I’ve collaborated with Peter off and on for a long time. Peter works now as a consultant. He has his own consultancy company in southern England. And he also does some academic tutoring for Oxford and other universities. We have a long-term collaboration. We’re both interested in how biodiversity changes through time
HS: What was the motivation to sample diversity at the power station?
AM: Peter originally worked for the Central Electricity Generating Board, which at that time was a nationalized company owned by the British government, responsible for generating electricity. And as part of that, he was one of their biologists charged with environmental monitoring which included collecting data on the biological diversity associated with power stations. I think that was the initial motivation for the sampling. After the service was privatized, he set himself up as a consultancy business; and he’s been able to continue to collect the data as part of that.
But as I said, it’s a very strong testament to his commitment that he’s managed to do this. He’s supported the data collection through his own efforts, rather than funded by research grants.
HS: Stepping back a bit, I wanted to ask you how you got interested in biodiversity, especially the measurement of biodiversity. From your publication profile, I realize that there you have two broad research interests: fish behavior and biodiversity. And it seems like, initially, you did a lot of work on fish behavior, and I think around 1988 was when you started, or at least your first paper and the book on biodiversity, was around the late 80s. Can you tell us a little bit about how these different interests came about?
AM: Well, in fact, I first started working on biological diversity. I went to university in Northern Ireland and my PhD was on biodiversity in forests. I compared the diversity of natural oak woods and coniferous plantations in Northern Ireland. My goal was measuring biodiversity and trying to understand the best ways to quantify it. But this was a time when it was very difficult to get academic jobs, as it was during the period when Margaret Thatcher had a big influence on universities, and there were many cut backs. So, after my PhD, I switched to working on fish behavior because that was an opportunity that was available to me at the time in a very difficult job market. I worked on fish behavior for many years, but I kept up my interest in biodiversity measurement at the same time. I wrote my first book at that stage; it was on biodiversity measurement and was based heavily on my PhD thesis. As time has gone on, I’ve started to focus more on biodiversity, and I’m not doing much fish behavior work at all at the moment.
HS: Could you tell us a little bit about how you actually worked with Peter Henderson for this paper? Do you remember when and where you and Peter did the analysis and the writing up?
AM: We met up very occasionally, and I visited him near Southampton, when we were writing it up. Mostly we used email.
HS: Do you remember, roughly, how long it took you to write the paper?
AM: About six months.
HS: Did this paper have a relatively smooth ride through peer review? Was Nature the first place you submitted this to?
AM: It was published in April. I recall we submitted it in the autumn and it went to review. And then we had to do one set of revisions. I think that was it. Maybe some final clarifications, but it was relatively smooth sailing. Often, it’s very difficult to get papers published. That one was relatively smooth sailing.
HS: You thank R. Seeby and R. Somes for help with fieldwork. Who were these people?
AM: They were Peter’s colleagues who work with him in his consultancy firm, Pisces Conservation https://consult.pisces-conservation.com/. Fieldwork is arduous and needs several people.
HS: At the time when the paper was published, do you remember if it attracted a lot of attention, within academia and from the popular press?
AM: It attracted quite a lot of attention from others ecologists and it has been very well-cited which is nice. I don’t think it attracted any attention from the press.
HS: Did this paper have any kind of direct impact on your career?
AM: Yes, it has been helpful, and probably contributed to getting grants and awards. So yes, of course it’s been positive. But the fundamental reason for doing the work is because we were curious about how ecosystems are structured and how they change. The main influence of the paper has been to inspire new questions and challenges that have kept me busy ever since.
HS: Did the paper have an influence on the future trajectory of your research itself, i.e. did you follow up on this in any way?
AM: Yes, it absolutely did. One thing I did after that was to apply for funding from the European Research Council for an advanced grant, which I was very fortunate to get. That advanced grant was called BioTIME, and the aim of BioTIME was to understand how biodiversity changes through time. That was definitely something that followed on from the work in this paper.The paper, for me, opened up quite an important research theme, which I’m still working on. We were very fortunate as well because we recognized the importance of understanding temporal change in biodiversity quite early on.
HS: Today, 13 years since this paper was published, would you say that the main conclusions from the paper still hold true, more-or-less?
AM: Oh yes, I think this is a strong finding. In fact, this morning I was thinking that we should go back and update the analyses, because it’s been over 30 years. But I do know that the main patterns are still there. In the paper, we talked about the possibility that some species would become more common because of changes in water temperature and others would become rarer; I’m pretty sure that’s what’s happened. I did some follow up work a few years back, with other colleagues, in a paper published in Nature Communications. This paper looked at changes in fish populations in the waters of west Scotland and revealed a signature of climate change affecting the distributions of fish. So it’s a long answer to the question, but yes, there’s been lots of follow-up.
HS: In the paper you say, “As the time series lengthens we expect the modes of the two distributions to move apart and the division zone to become broader and clearer”. Is this something that you have looked at, or plan to look at, with more recent data?
AM: We’ve looked at it informally. But this conversation is very good motivation to me to look at it more formally. But I’m pretty sure that’s the correct take on what’s happening.
HS: You also say, “Species are also lost over longer timescales: in our study area the eel (Anguilla anguilla) is currently declining and might shortly become an occasional visitor rather than a member of the core community”. Do you know if that’s happened?
AM: Eels are very infrequent now. They are one of the species that have declined in abundance over time. And that, in fact, is true, right through the north Atlantic.
HS: Towards the end of the paper, you say, “If conditions alter sufficiently we predict that new core species, drawn from the pool of occasional species, will replace the existing ones.” It’ll be interesting to see if that’s actually the case…
AM: That’s correct. I’m not sure that that’s happened yet, but I think it certainly would do if conditions change enough. In the Bristol Channel the water temperature increased for a few years, and then cooled for a few years. These changes have resulted in a little bit of reorganization amongst the core species and amongst the rare species, but we haven’t seen any major restructuring of the community yet. In other fish communities there will be larger changes, linked to long term directional changes in temperature.
HS: Finally you say, “Temporal components of species abundance also have important implications for conservation planning, as recognized by the latest generation of reserve selection algorithms.” More recently, have you seen this happen, i.e. temporal patterns being incorporated more in conservation planning and algorithms for reserve design?
AM: I think there’s still a way to go before that’s going to happen but more people do recognise its importance. My colleagues and I have papers in Science and some other journals looking at biodiversity change in assemblages throughout the world. These have made it very clear that compositional change is a crucial factor that needs to be considered in conservation. Not much has happened yet. But one thing that is happening is that the IPBES initiative is looking for ways of monitoring biodiversity and biodiversity change, and they are beginning to take compositional data much more into account. So yes, it is beginning to happen.
HS: If you were to redo this study or re-analyze this dataset today, would you do anything differently? Has your thinking on these ideas changed in any way in the last 13 years?
AM: Not really. Of course, there are better ways of fitting species abundance distributions, so the statistical analysis would be a little bit more refined. But I don’t think, conceptually, it would be very different.
HS: Can you tell us a little more about that? In what ways would you would the statistics be different?
AM: Well, then we fitted some log-normal distributions and log-series distributions just using a conventional method of regular goodness-of-fit statistics. But now there are more powerful model selection statistics, which can be used, and would strengthen insights into how well different distributions fit. That said, I don’t think it would change our conclusions about the patterns that we saw.
HS: Like you mentioned earlier, this paper has been very well-cited. Do you have a sense of what it mostly gets cited for?
AM: Oh, not really. In ecology there are a lot of quite complex patterns, and explaining patterns in biodiversity remains a major challenge. But this was quite a simple straightforward pattern, and I think it appeals to people for that reason. And it’s something that you can see in many different assemblages. For example, I was an external examiner on a PhD thesis recently, where the student had looked at microbial communities. One of the things that he was testing was whether or not this pattern of core and transient species was present in his data; and it was. So it’s something that can be applied to lots of different systems, and it’s a clear pattern to look for.
HS: In the 13 years since this paper has been published, have you ever read the paper again?
AM: I read it this morning! But, occasionally, yes.
HS: In what context have you read it?
AM: I’ll probably just check some details of the analysis. If we’re doing some other work, just to make sure that what was said the last time is consistent with my memory of it; that’s all.
HS: When you compare this paper to papers you write today, do you notice any striking differences?
AM: These days, we tend to have a lot more material in the supplementary material section. I don’t think we had any supplementary material; this is very short paper. But these days, you’re expected to provide much more background support for your analyses and so on. That’s one big difference.
HS: When you read the paper this morning, what was your reaction to it? Was there anything that you struck you about the paper?
AM: It was quite enjoyable to read it again. There was more analysis than I remembered. I really tend to think of the very central conclusion of the distinction between the core and the transient species. I forgot that we had done additional analysis to bolster that, which I think was something that was requested by referees. I’d forgotten the details of that. But, in general, the paper was quite nice to read it again.
HS: Would you count this as one of your favorites among all the papers you’ve published?
AM: Oh yes.
HS: And can you tell us a little more about what you like about this piece of work?
AM: When we started to look at the data, the finding just really popped out. And it is a nice, clear result. So that’s very pleasing
HS: What would you say to a student who’s about to read this paper today? What should he or she take away from this paper publish 13 years ago? Would you add any caveats?
AM: Ah. I guess I would say that to understand ecology, you have to understand the systems that you’re working with. Our advantage was that both Peter and I do a lot of fish biology. So we were quite well-equipped to understand the ecology that that was inherent in the system, and I think that made a big contribution. What would I tell students to do? I would say it’s just a small study that illustrated a particular point. And it’s not the last word on the subject by any means. There’s still a lot of analysis to be done. And many other systems and the conservation angle are still out there to be explored. I guess I’d say that. It’s not a very good answer, but it’s a hard question!
HS: One last question. Do species rarity and species abundance distributions continue to be important areas of research for you?
AM: Absolutely, yes. I think there are lots of questions that we still haven’t answered.
HS: Do you continue to do, both, theoretical and empirical work on these topics?
AM: Most of my recent work has focused on analysing biodiversity time series. I’ve been working a lot in Trinidad, for example. We have a nice dataset from Trinidadian rivers, and are trying to understand the patterns there. It’s a data-driven understanding of ecology rather than the theoretical approach to ecology.