A slightly less paradoxical paradox

All organisms are built from the same recipe of 25 or so elements, and so it makes sense that as you increase the supply of those building blocks to an ecosystem, you should be able to increase the number and variety of organisms that ecosystem supports. Deserts vs. rainforests, right? In a paper just out from a terrific collaboration,  we show, it turns out, things are not quite that simple.

The background

Michael Rosenzweig

Michael Rosenzweig

In 1971, Michael Rosenzweig (MikeK’s Ph. D. advisor and friend of the Kaspari lab) used a suite of differential equation models to explore why adding nutrients to an ecosystem so often reduced, not enhanced, the number of species. He coined the term “Paradox of Enrichment” to capture this incongruity. Since then Rosenzweig and a who’s who of ecologists–particularly terrestrial botanists–have documented this Paradox and compiled a long list of mechanisms that could explain it.

A few years ago, our lab joined a team of collaborators to take on the relationship between nutrient availability and diversity in tropical soils. We did so using a grand experiment initiated by Joe Wright and colleagues at the Smithsonian Tropical Research Institute in Panama.  Since 1998, we have been fertilizing 40×40 m plots with the “big 3” nutrients–Nitrogen, Phosphorus, and Potassium–as well as a cocktail of micronutrients from Boron to Zinc. In 2012, as part of an NSF MacroSystems grant, we visited each of these plots, sampled soil and litter, and used a variety of molecular and traditional methods to count the number of species of bacteria, fungi, and invertebrates on the essentially 9 different kinds of tropical soils generated by this experiment.  I would say that our results, out early online in the journal Ecology, were surprising, but, what happens when you quantify the absence of a paradox?

Gigante Fertilization Experiment

The Gigante Fertilization Experiment, one of the largest, and longest running such planned experiments on Earth. (You can say that humans are actually doing a pretty good job of adding Nitrogen and Phosphorus and a variety of metals to Earth’s ecosystems in a less scientific, tho none-the-less deliberate manner).

The results are wonderfully complex, but here are some highlights.

Bacteria, Fungi, and Invertebrates each had their own “biogeochemical niche”.

If you plot out the magnitude of diversity responses to nutrients–positive or negative–the resulting fingerprint differed among the big three soil supertaxa. Everybody’s diversity suffered when nitrogen alone was added. This is as close as you get to a uniform Paradox of Enrichment. After that, Bacteria increased the most (and modestly) with phosphorus (P), fungi were all over the map but tend to do better with potassium (K), and invertebrates showed the biggest increases when combinations of nutrients were applied.

Why does nitrogen do a number on soil diversity?  The standard explanation is that there are a handful of weedy taxa that just thrive when nitrogen is superabundant (fertilize a prairie with urea and you wind up with tall, green patch of invasive grass). But we find little evidence for that: things that increase on N plots tend to be rare, and increase when any nutrient is added (and some of them are icky. See below).

Instead, we suggest that nitrogen, which tends to acidify the soil, sets off a chain reaction by which aluminum–a toxin to most life–leaches into the water supply and bathes the unfortunate members of the brown food web in a bath of metal. In other words, nitrogen doesn’t seem to favor a suite of nitrogen specialists, it releases an all-purpose toxin that stresses everybody out.  That’s our new working hypothesis. It needs to be tested.

Fig 1 Richness ES w treatment.JPG

A summary of our results. The Effect Size is a way of uniformly expressing the change in diversity, positive or negative ,of a fertilizer compared to unfertilized plots. For example,  fertilizers tend to have a bigger effect on invertebrates than bacteria. More and more complex fertilizer combos are arrayed toward the right. 

Combo’s of nutrients often enhance diversity more than individual nutrients.

One common pattern among plants is that if adding one nutrient, say nitrogen, drops diversity in a prairie, adding two, say nitrogen and phosphorus, does so even more. We don’t find much evidence for that. Instead, the two groups with big, complicated genomes–the fungi and invertebrates–show the largest increase in species diversity when micronutrients are added. Invertebrates do almost as well when the big three nutrients, N, P, and K, are added in tandem. What is it about nutrient combos that favor mushrooms and ants?

We suggest that one reason is that critters with large genomes need a ready supply of chemical elements to build and maintain their more complex metabolisms. It is fun to ponder such a link between an organism’s metabolic diversity–the number of enzymes it has linked together in intricate pathways (many of which require a metal like Zinc or Copper to operate properly) and its metal-craving. Again, this is a working hypothesis. But we have already shown that decomposition in this system–the combined action of the metabolisms of the brown food web–shows big increases on the +Micronutrient plots in the Gigante experiment.

Of the three soil supertaxa, the bacteria and invertebrates have the most similar biogeochemical niches.

One might have guessed that fungi and bacteria–both “microbes” that break down “detritus”*–might respond similarly to the same nutrients, but this doesn’t seem to be the case. Fertilizers with a strong effect on bacterial diversity tended to have little effect on fungi, and visa versa. On the other hand, the fertilizers that really knocked down bacterial diversity, N and NK, did the same for invertebrates.

Many soil inverts have rich microbiomes in their guts that allow them to make a living in the brown food web. Could this be one cause of their similar responses. Does the gut flora of millipedes also suffer in bacteria-poor soil?

Fig 2 Covariance of Diversity Responses

When you contrast the effect of a fertilizer on diversity between each combo of the soil supertaxa, fungi and prokaryotes (bacteria) do their own thing, while bacteria and invertebrates tend to response more similarly. 

There are weedy taxa in each of the three supertaxa

Which taxa thrive regardless of what nutrient you drop on the soil? It is somehow satisfying to find that among the invertebrates, the Blattaria (aka roaches) can’t say no to any fertilizer.

It is a little more chilling that among the fungi, only the Chytrids, a phylum that contains the infamous B. dendrobaditis, a deadly pathogen of amphibians, increases in diversity in response to almost any fertilizer.  We are fertilizing the planet. Just a pattern thus far. Someone should look into it.

Fig S1 Effect sizes by subclades

Subtaxa of the soil supertaxa that respond positively or negatively to a given fertilizer by at least one standard deviation over controls. See paper to suss out all the abrev’s.

What’s the take home?

Humans are rearranging Earth’s biogeochemistry–depleting fertile soils through erosion and dumping enormous quantities of N, P, and C and a mess of metals into the biosphere. Our study contrasted three grand hypotheses for how fertilization shapes diversity–by increasing abundance, by favoring a subset of competitive species, or by acting as toxins. Much of what we ecologists know about these nutrient effects comes from the experiments of our botanical colleagues. And those experiments consistently point to fertilizers favoring a subset of high-nutrient specialists that drive other species locally extinct. The Paradox of Enrichment is thus an inevitable result of simplifying the environment with fertilizers to favor a handful of species.

But by focusing on three soil supertaxa–the bacteria**, fungi, and invertebrates–that account for most of the diversity of life on dry land, we find evidence for some nutrients enhancing abundance, others acting as toxins and for combos of nutrients ameliorating toxic effects. For some of the reasons why, check out our Discussion. Not surprisingly, spatial scale comes into play. And how metabolisms are rejiggered.

An enduring question is how the combined diversity of life in any given ecosystem–from trees to mites to microbes–will respond to the slings and arrows of anthropocene fortune. The answer “it’s complex” shouldn’t surprise. At the same time, one path ahead, we think, lies in  contrasting how tiny organisms with effectively infinite population sizes and evolutionary potential to match respond to global change compared to their large colleagues that can be comfortably enumerated with m2 quadrats.


*Combining fungi with bacteria** as “microbial” is akin to combining petri dishes and planets as “matter-intensive phenomena”.  Likewise “detritus” can be anything from a dead leaf to a dead armadillo. *Celebrate* the diversity.

**Again, I beg forgiveness from microbial ecologists for using the shorthand “bacteria” or “prokaryotes” to lump together the archaea and eubacteria. I was raised by ornithologists.

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