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Posts Tagged ‘ecosystem services

A $3.8 trillion mistake, and why it (mostly) doesn’t matter

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The controversy over mistakes in a key paper used to justify austerity reminded me of what seems to be another simple mathematical mistake in a high profile paper. The authors of this paper tried to tot up the total value of the world’s ecosystem servicesthe ways that humans benefit from the natural world. This kind of valuation is pretty controversial: critics feel that putting a dollar value on nature misses the point and leaves some ecosystems vulnerable, while advocates argue that it’s the only realistic way to include nature in a discussion that all too often just looks at ‘the economy, stupid’.

Costanza et al. ran the figures for a whole range of ecosystem services, and estimated that we get some $33 trillion of value per year. The paper was published in Nature, and according to Google Scholar, has since been cited some 9488 times. I won’t discuss how they got all the numbers and what they mean; if you’re interested, have a look at the paper itself, and critiques such as this and this. My focus today is more specific.

Looking at the breakdown of values for different services and biomes (table 2), by far the largest single value is for nutrient cycling, described in table 1 as “storage, internal cycling, processing and acquisition of nutrients”, for example “nitrogen fixation, N, P and other elemental or nutrient cycles.” That’s mostly from marine systems: the total value of nutrient cycling by marine ecosystems appears to be $15.3 trillion per year, a little under half of the grand total. To get behind that number, we need to dive into the supplementary information. The relevant section reads:

We assumed that the oceans and coastal waters are serving as sinks to all the world’s water that flows from rivers, and that the receiving marine waters provide a nutrient cycling service. If we assume that roughly one-third of this service is provided by estuaries (Nixon et al. 1996 in press) and the remainder by coastal and open ocean, (assume 1/3 by shelf and 1/3 by ocean), then the total quantity of water treated is 40 x 1012 m3 y-1. Replacement costs to remove N and P were estimated at $0.15 – 0.42 m-3 (Richard et al. 1991 as quoted in Postel and Carpenter 1997). Thus, the replacement cost for each biome’s (1/3) contribution to the total value is $2.0 x 1012–$5.6 x 1012. By hectare, the value for ocean (32200 x 106 ha) is then $62.1 – 174 ha-1 y-1.

First, where does that total quantity of water come from? It looks like it should be the total flow of the world’s rivers, and this Russian paper from 1993 confirms that, putting total river runoff at 42,700 km3 per year, about the same as the volume given. I’m not entirely sure about this way of calculating replacement valueif we had to recycle those nutrients ourselves, wouldn’t we find a more efficient way than filtering them out of all the world’s rivers?but let’s accept the assumptions for now.

Multiplying the total volume by the estimated treatment values (15 to 42 ¢ per cubic metre) gives us $6.0–16.8 trillion, a range with a midpoint of $11.4 trillion. That’s quite a bit lower than the value $15.3 trillion total we got for nutrient cycling in the oceans above. Where has the extra come from?

As the quotation mentions, the authors assume that three biomesestuaries, the continental shelf and river estuarieseach perform a roughly equal amount of that nutrient cycling. So the total value is split into three chunks of $3.8 trillion, one assigned to each ecosystem. But then a fourth chunk of $3.8 trillion turns up, assigned to seagrass & algae beds (and by itself making those the third most valuable biome per hectare). The notes for nutrient cycling in this biome just say “For calculation methods, see notes for Ocean.” I can only guess that the authors decided that seagrass and algae beds had an important role in recycling nitrogen and phosphorus, but forgot to recalculate it to split the total over four biomes.

section of Costanza et al table 2

The extra number (from table 2 of the paper). These figures are US dollars per hectare per year.

I’ve checked over this several times, and when I first spotted it, I bounced it off one of my professors, although unfortunately I no longer have the e-mails. If I’m wrong, I hope the authors will accept my apologies. But even in that case, I don’t think that the information in the paper and the supplementary information clearly justify these numbers, which make up the biggest part of the headline figure.

Of course, unlike in the austerity paper, this doesn’t really affect the conclusions of the study. Whether the central figure is $33 trillion or $29 trillion, it’s clearly enormous: the authors highlight that it’s more than the world’s GNP ($18 trillion in 1997, when the paper came out). And that number is just the centre of a range of $16–54 trillion, so there was already plenty of uncertainty. More importantly, it’s probably an underestimate, because of all kinds of services and factors that couldn’t be included in the analysis. It’s clear that we benefit immensely from the natural world.

So is this $3.8 trillion dollar slip wholly unimportant? Why am I writing about it? Well, I don’t think it’s a great testament to the peer review process. All the information to spot this was there in the supplementary information, but even for a paper in the world’s most prominent journal, reviewers apparently didn’t reach for a calculator and check through the numbers. Happily there are moves afoot to improve reproducibility, and people are working on better tools for scientific computing. But how many other papers out there have simple mistakes in the numbers?

But I’d prefer to look at this more optimistically. Like Thomas Herndon, who dug out the Excel mistake in the now-infamous Reinhart & Rogoff paper, I spotted this while I was an undergraduate, reading about ecosystem services for my conservation module. Checking a calculation is a lot easier than finding and justifying all the numbers in the first place, and there are plenty of undergrads ;-). We might not be able to replicate every lab experiment, but re-checking published calculations is well within the realm of possibility.

The paper in question:

Costanza, R., d’Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., O’Neill, R., Paruelo, J., Raskin, R., Sutton, P., & van den Belt, M. (1997). The value of the world’s ecosystem services and natural capital Nature, 387 (6630), 253-260 DOI: 10.1038/387253a0

The supplementary information no longer seems to be on the Nature website, but there’s a copy linked from this Duke University page.

Written by Thomas Kluyver

26 April, 2013 at 11:17 pm

Posted in Papers

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Is climate change affecting phytoplankton?

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Phytoplankton—single celled green floaters—fulfil the same role in the oceans as plants do on land. They’re the basis of the food chain, capturing energy from sunlight, and eventually feeding just about everything else. So the news that they’ve declined by about 40% since 1950 (Nature News) is rather worrying. Let’s take a look at where the number came from.

Black and white disk, suspended above water.

A Secchi disk. Photo from eutrophication&hypoxia (flickr)

The standard way of finding the amount of phytoplankton in seawater is to measure the concentration of chlorophyll, the green pigment used in photosynthesis. Essentially, you can just test how green the water is, although modern methods are a bit cleverer. Using satellites, you can even remotely measure vast areas of ocean. But people didn’t make those measurements much until the 1960s (and not with satellites until 1979). So the researchers combined them with an even simpler method, which has been done a lot since the 1930s. The ‘Secchi disk’ is lowered into the water until it can no longer be seen, giving a measure of how clear the water is. After throwing out measurements near the shore, where mud can reduce visibility, they fit pretty well with the chlorophyll measurements.

What did they find? Well, the number the media picked up on was the global average 1% decline per year. That’s one percent of current levels, so working back gives you just under a 40% drop since 1950. That average, though, hides quite a bit of variation in the actual change:

Graph of the historic changes in chlorophyll in eight regions of the global ocean.

Changes in phytoplankton (chlorophyll concentration). Based on a figure in the paper, with minor modifications.

It looks like there’s a clear decline in the Atlantic ocean and the polar oceans, a smaller decline in the Pacific, while plankton actually increased in the Indian ocean. The authors go one step further, breaking it down into large grid squares. That shows still more variation, but without a clear pattern, at least to my eye.

I mentioned a link with climate change. It works like this: when you heat a pan of water on a stove, you get convection currents, as warm water rises, cools, and sinks again. But the oceans are mostly heated from the top, by sunlight, which means a layer of warm water forms, sitting on top of a huge depth of colder water. Phytoplankton can only grow near the surface, because they need sunlight, but they quickly use up the nutrients there, and then need water mixed in from the depths to grow. As a result, regions of upwelling water, such as off the coasts of Peru and Antarctica, have particularly rich sea life. The ocean currents that drive them aren’t expected to stop any time soon, but warmer temperatures at the surface could be reducing smaller scale mixing.

This isn’t just conjecture. The scientists separated the year-by-year variation in plankton levels from the overall trends, and compared that variation to various ocean ‘oscillations’. These are roughly regular patterns in temperature and pressure, the best known of which is the El Niño/Southern Oscillation in the Pacific. In most areas with oscillations, there was less plankton in warmer years (the pattern didn’t fit for the North Indian ocean, perhaps due to the effects of the monsoon rains).

I’m a bit surprised, reading the paper, that they didn’t explore any of the other things that could be affecting the plankton. There’s a brief list of possible factors, including nutrients coming from the land, ocean circulation, and the effects of other organisms in the sea, but then only the surface temperature and the resulting ‘mixed layer depth’ are given any discussion at all.

If phytoplankton are on the decline due to global warming, that’s not just bad news for the algae. As I described above, almost* everything in the oceans ultimately relies on phytoplankton. They’re also a key part of the carbon cycle, removing CO2 from the air. That leads to a positive feedback: as we release more CO2 and warm the earth, we also slow down its absorption by life in the oceans.


Boyce, D., Lewis, M., & Worm, B. (2010). Global phytoplankton decline over the past century Nature, 466 (7306), 591-596 DOI: 10.1038/nature09268

*Treasure your exceptions: some things living at hydrothermal vents can get all their energy from dissolved chemicals.

Written by Thomas Kluyver

6 August, 2010 at 11:56 pm

Do bees benefit from a balanced diet?

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We discussed this paper at a journal club in our department yesterday (Monday 1st February). Some of our thoughts are below.

Although the media coverage of this study played heavily on the link to colony collapse disorder (which is causing honeybee colonies to die off around the world), the authors only allude to it in one sentence near the end. The study tries to show that bees fed a mixture of pollen from different plants are healthier than those fed only one type of pollen, which is interesting because modern farming tends to create large areas of just one species. It’s not entirely convincing, though: of the four things they measure, only one (glucose oxidase) convincingly shows that pattern, and even that’s not a terribly dramatic difference (see the graph). The researchers deserve kudos for showing all four results, even though I’ve just picked out one here:

Bar chart of glucose oxidase levels in bees fed different pollen diets.

Glucose oxidase levels in bees fed different diets. The highlighted two bars on the right are from the mixed diets, the 'control' on the left had a diet without pollen, and the other four were fed one type of pollen each. Numbers underneath are the proportion of protein in the pollen. From Alaux et al. 2010.

Interestingly, glucose oxidase is used as an antiseptic, to kill off bacteria in honey and food for the larvae. So it’s colony defence against disease that is improved, not just the individual bees’ resistance.

Much of our discussion focussed on the methods, which leave something to be desired. The two pollen mixtures both included two types of pollen (willow and maple) which weren’t in any of the single-pollen diets, so the apparent effect of blending pollen could be down to something in one of those types. We also questioned whether the pollen sources are relevant to what bees naturally eat. Some of them are wind-pollinated trees, which sounded counterintuitive, but in fact I can find most of the plants in a list of bee pollen sources, and the French company that supplied the pollen actually collects it from beehives.

The experiment didn’t run for very long, at just ten days, and was only done on adult bees, while a bee’s diet as a larva could have important effects. This might go some way to explain why the differences between groups are fairly small. Ideally, it would be interesting to limit the pollen available to entire hives for a full generation and study the effects, although that would take much more time and funding. It would also be good to look at how the differences in ‘immunocompetence’ measured here relate to the bees’ response to a disease. The study mentions a couple of papers which have looked at diet and immune responses, although neither of them are in bees.

Moving on to the results of the study, we mentioned that the different parts of the immune system may be involved in trade-offs; the more of one thing a bee makes, the less it can produce of another. So it might be interesting to combine the four different variables measured into a general pattern, and then look at how diet affects that; although of course that shouldn’t get in the way of publishing the simple data.

Among their results, one measure, the count of haemocytes (which are kind of like white blood cells), did something unexpected: it went up in the control bees, which were fed no pollen. There are different types of haemocytes, and not all of them are involved in immunity, but it’s still an odd result. The study suggests that perhaps the greater number is compensating for something, for example if each cell is less active, but it didn’t strike me as convincing.

Although the researchers focussed on the protein in the pollen, we reckoned that the effect of mixed-pollen diets was more likely to hinge on micronutrients such as vitamins, since they’re numerous, and perhaps no one type of pollen would contain them all.

Finally, a few of our more speculative thoughts:

  • How does this affect solitary bees, which by definition don’t have a hive to protect? Solitary bees are probably important pollinators for many wild species, whereas honey bees are used commercially to pollinate many crop species, especially fruits.
  • Does the ‘hygiene hypothesis’ (that the immune system goes wrong if it’s not exposed to diseases and can’t ‘learn’ about them) apply to bees? Microbial symbionts might help about against disease, but could spraying of hives with antibiotics have killed off the symbionts, leaving the bees more vulnerable?
  • Glucose oxidase and phenol oxidase (another thing which was measured) probably increase as bees get older; could the different pollen diets have been affecting how quickly the bees aged?
  • Do worker bees have different castes, and would their diets differ? A bit of searching suggests that they change tasks over their lifespan of a few weeks (‘temporal castes’ to use the technical term; see this paper), starting out inside the hive and ending up as foragers. It’s possible that foragers (older bees) have a less varied diet, if they only eat what they collect, while the bees in the hive dine on pollen from many foragers, but this is entirely guesswork.


Alaux, C., Ducloz, F., Crauser, D., & Le Conte, Y. (2010). Diet effects on honeybee immunocompetence Biology Letters DOI: 10.1098/rsbl.2009.0986

Written by Thomas Kluyver

2 February, 2010 at 11:06 pm

Posted in Papers

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