Bacteria & archaea don't get no respect from interesting but flawed #PLoSBio paper on # of species on the planet

Uggh. Double uggh. No no. My first blog quadruple uggh. There is an interesting new paper in PLoS Biology published today. Entitled "How many Species Are There on Earth and in the Ocean?" PLoS Biol 9(8): e1001127 - it is by Camilo Mora, Derek Tittensor, Sina Adl, Alastair Simpson and Boris Worm. It is accompanied by a commentary by none other than Robert May, one of the greatest Ecologists of all time: PLoS Biology: Why Worry about How Many Species and Their Loss?

I note - I found out about this paper from Carl Zimmer who asked me if I had any comments.  Boy did I.  And Zimmer has a New York Times article today discussing the paper: How Many Species on Earth? It’s Tricky.  Here are my thoughts that I wrote down without seeing Carl's article, which I will look at in a minute.

The new paper takes a novel approach to estimating the number of species. I would summarize it but May does a pretty good job:

"Mora et al. [4] offer an interesting new approach to estimating the total number of distinct eukaryotic species alive on earth today. They begin with an excellent survey of the wide variety of previous estimates, which give a range of different numbers in the broad interval 3 to 100 million species"

....

"Mora et al.'s imaginative new approach begins by looking at the hierarchy of taxonomic categories, from the details of species and genera, through orders and classes, to phyla and kingdoms. They documented the fact that for eukaryotes, the higher taxonomic categories are “much more completely described than lower levels”, which in retrospect is perhaps not surprising. They also show that, within well-known taxonomic groups, the relative numbers of species assigned to phylum, class, order, family, genus, and species follow consistent patterns. If one assumes these predictable patterns also hold for less well-studied groups, the more secure information about phyla and class can be used to estimate the total number of distinct species within a given group."

The approach is novel and shows what appears to be some promise and robustness for certain multicellular eukaryotes. For example, analysis of animals shows a reasonable leveling off for many taxonomic levels:

Figure 1. Predicting the global number of species in Animalia from their higher taxonomy. (A–F) The temporal accumulation of taxa (black lines) and the frequency of the multimodel fits to all starting years selected (graded colors). The horizontal dashed lines indicate the consensus asymptotic number of taxa, and the horizontal grey area its consensus standard error. (G) Relationship between the consensus asymptotic number of higher taxa and the numerical hierarchy of each taxonomic rank. Black circles represent the consensus asymptotes, green circles the catalogued number of taxa, and the box at the species level indicates the 95% confidence interval around the predicted number of species (see Materials and Methods).
From Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B (2011) How Many Species Are There on Earth and in the Ocean? PLoS Biol 9(8): e1001127. doi:10.1371/journal.pbio.1001127

They also do a decent job of testing their use of higher taxon discovery to estimate number of species.  Figure 2 shows this pretty well.

Figure 2. Validating the higher taxon approach. We compared the number of species estimated from the higher taxon approach implemented here to the known number of species in relatively well-studied taxonomic groups as derived from published sources [37]. We also used estimations from multimodel averaging from species accumulation curves for taxa with near-complete inventories. Vertical lines indicate the range of variation in the number of species from different sources. The dotted line indicates the 1∶1 ratio. Note that published species numbers (y-axis values) are mostly derived from expert approximations for well-known groups; hence there is a possibility that those estimates are subject to biases arising from synonyms.

So all seems hunky dory and pretty interesting.  That is, until we get to the bacteria and archaea.  For example, check out Table 2:

Table 2. Currently catalogued and predicted total number of species on Earth and in the ocean.

Their approach leads to an estimate of 455 ± 160 Archaea on Earth and 1 in the ocean.  Yes, one in the ocean.  Amazing.  Completely silly too.  Bacteria are a little better.  An estimate of 9,680 ± 3,470 on Earth and 1,,320 ±436 in the oceans.  Still completely silly.

Now the authors do admit to some challenges with bacteria and archaea. For example:

We also applied the approach to prokaryotes; unfortunately, the steady pace of description of taxa at all taxonomic ranks precluded the calculation of asymptotes for higher taxa (Figure S1). Thus, we used raw numbers of higher taxa (rather than asymptotic estimates) for prokaryotes, and as such our estimates represent only lower bounds on the diversity in this group. Our approach predicted a lower bound of ~10,100 species of prokaryotes, of which ~1,320 are marine. It is important to note that for prokaryotes, the species concept tolerates a much higher degree of genetic dissimilarity than in most eukaryotes [26],[27]; additionally, due to horizontal gene transfers among phylogenetic clades, species take longer to isolate in prokaryotes than in eukaryotes, and thus the former species are much older than the latter [26],[27]; as a result the number of described species of prokaryotes is small (only ~10,000 species are currently accepted).

But this is not remotely good enough from my point of view. Their estimates of ~ 10,000 or so bacteria and archaea on the planet are so completely out of touch in my opinion that this calls into question the validity of their method for bacteria and archaea at all. 

Now you may ask - why do I think this is out of touch. Well because reasonable estimates are more on the order or millions or hundreds of millions, not tens of thousands. To help people feel their way through the literature on this I have created a Mendeley group where I am posting some references worth checking out.

Number of species of bacteria and archaea is a group in Biological Sciences on Mendeley.

I think it is definitely worth looking at those papers.  But just for the record, some quotes might be useful.  For example, Dan Dykhuizen writes

we estimate that there are about 20,000 common species and 500,000 rare species in a small quantity of soil or about a half million species.

And Curtis et al write:

We are also able to speculate about diversity at a larger scale, thus the entire bacterial diversity of the sea may be unlikely to exceed 2 × 10^6, while a ton of soil could contain 4 × 10^6 different taxa.

Are their estimates perfect?  No surely not.  But I think without a doubt the number of bacterial and archaeal species on the planet is in the range of millions upon millions upon millions.  10,000 is clearly not even close.  Sure, we do not all agree on what a bacterial or archaeal species is.  But with just about ANY definition I have heard, I think we would still count millions.

Given how horribly horribly off their estimates are for bacteria and archaea, I think it would have been better to be more explicit in admitting that their method probably simply does not work for such taxa right now.  Instead, they took the approach of saying this is a "lower bound".  Sure.  That is one way of dealing with this.  But that is like saying "Dinosaurs lived at least 500 years ago" or "There are at least 10 people living in New York City" or "Hiking the Appalachian Trail will take at least two days."  Lower bounds are only useful when they provide some new insight.  This lower bound did not provide any.

Mind you, I like the paper.  The parts on eukaryotes seem quite novel and useful.  But the parts of bacteria and archaea are painful.  Really really painful.

Mora, C., Tittensor, D., Adl, S., Simpson, A., & Worm, B. (2011). How Many Species Are There on Earth and in the Ocean? PLoS Biology, 9 (8) DOI: 10.1371/journal.pbio.1001127