Monday, May 11, 2015

Is there a limit to how many species can the earth hold?

Counting species (bird lists, plant guides) is as old as ecology itself. And yet surprisingly, there are still different opinions on how many species the planet holds, and even, whether there are limits on how many species it can have. If the number of species has ecological limits, the assumptions ecologists often make – that species pools are limited and knowable, dynamics can reach equilibrium, competition should usually be important – would be stronger. Things would be more predictable. 

But is the production of diversity self-limited? There isn’t consensus but two recent articles in the American Naturalist (continuing a debate at the American Society of Naturalists meeting) provide some excellent debate of this question.

The debate is whether the majority of variation in continental-scale species richness is regulated by diversity-dependent feedbacks. In these papers, Dan Rabosky and Allen Hurlburt argue that species richness has ecological limits, while Luke Harmon and Susan Harrison take the contrary position, that species richness is dynamic. First, to define some terms: here, species richness is being considered at the largest spatial scale (e.g. terrestrial plants at the continental scale) so that dispersal limitation should be comparatively unimportant (because diversity changes are mostly driven by in situ speciation).

The crux of the Rabosky & Hurlburt argument is established in the Ecological Limits Hypothesis (ELH), which states that species richness will reach a dynamic (i.e. stochastic) equilibrium, where equilibrium richness reflects density dependence in speciation and/or extinction rates. Speciation and extinction rates are ultimately limited by total resource availability for the continent. Therefore variance in richness through time and between places should be driven these ecological limits, and richness should be predictable.
From Rabosky & Hurlburt 2015 - the Ecological Limit Hypothesis.
The evidence presented for the ELH comes from phylogenies and macroevolutionary models, the fossil record, and macroecological observations. First, there are well known patterns between species richness and energy, productivity, or habitat area, and these span multiple regions and groups of species (e.g. Jetz and Fine 2012). Further, Rabosky & Hurlburt argue that geological records suggest that changes in diversity are not unbounded or exponential, but instead rise and fall, correcting toward some equilibrium. Molecular phylogenies are often evaluated by looking at speciation rates over time, and the authors suggest that these frequently show declines, where speciation declines during adaptive radiations. One prediction that arises from the ELH is that perturbations will be followed by particular responses: “negative perturbations—mass extinctions, in particular—should lead to diversity recoveries. Second, positive perturbations—increases in the resource base available to a biota—predict increases in species richness to stable but greater equilibrial levels”.

The rebuttal article from Harmon & Harrison takes a strong and contrasting view, although it focuses mostly on poking holes into Rabosky & Hurlburt’s arguments, rather than laying out a competing hypothesis. If Rabosky & Hurlburt focused on evidence over huge evolutionary scales and spatial expanses, the Harmon & Harrison response has a particular interest in the temporal and spatial scales of interest to community ecologists (local, present day) and how these seem to disagree with Rabosky & Hurlburt's hypothesis.

First, Harmon & Harrison argue that that the macroevolutionary evidence (molecular phylogenies, fossil data) is not nearly so convincing as Rabosky & Hurlburt suggest. There are important limits to its utility resulting from issues of ambiguity in interpretation and methodological limitations. In addition, for most of the patterns Rabosky & Hurlburt highlight, there are other papers concluding that the pattern was not present in their data. With reference to the lack of relationship between clade age and diversity: “A common interpretation of these results is that a lack of a relationship between age and diversity is evidence for ecological limits.... However… this pattern is far from ubiquitous in real data and is compatible with other explanations”. They also take issue with the tendency for hand-wave-y interpretations of patterns in such data, and emphasize the need for better statistical analyses and consideration of alternate models. Fossil data has obvious limitations as well (hence the field of taphonomy), including the fact that fossils are rarely classified to the species-level, which means they do not represent species richness, but rather lineage richness.

But Harmon & Harrison's real disagreement is based on their view that ecological evidence from local communities does not at all suggest ecological limits. Energy-richness correlations, although common, may have alternative explanations: the tropics may have higher diversification rates for other reasons, or niche conservation means that more species niches suited to the tropics, confounding energy-diversity relationships. Further, local communities do not regularly show a positive energy-diversity relationship. In particular, Harmon & Harrison suggest that the logic from the ELH, if followed, predicts that if species richness is ultimately tied to the availability of energy, then competition should necessarily be very important in most ecological communities. They cite a stat from the invasion of California flora in which alpha diversity has risen by more than 1000 invasive species, with only 28 native extinctions (as of 2002), suggesting that local (or even regional) communities are not full. 

To this, Rabosky & Hurlburt rejoins that invasion is about dispersal changes, and not resources. Further, they believe that large evolutionary scales are most useful as evidence for the ELH, since they are most likely to show zero sum game, rather than temporary dynamics, and since confounding factors should become minimized.

The debate left me feeling a little unsatisfied (since expecting the authors solve the problem is a bit unreasonable), in part because the authors are really arguing from different scales and approaches. And both sides are clearly right in some cases (and in others, perhaps, clearly overreaching). And of course, proving whether or not there is an ecological limit on diversity is a rather difficult thing. When Harmon and Harrison argue that the ELH, which assumes that richness approaches some equilibrium value but varies about it in a stochastic fashion, isn’t parsimonious, they’re wrong – ecological processes are innately stochastic and it hardly seem un-parsimonious to assume as much. But they’re right that this view makes testing and model fitting very difficult since having high replication and good quality data is necessary (to capture accurately a distribution, rather than single value). Given the variety of issues with data representing diversification over evolutionary time, and frequently an inability to capture extinction rates with evolutionary data, having quality, replicated tests of the ELH is difficult.

On the other hand, at local scales over ecological time, observations may be less relevant. It’s not clear how to reconcile statements about saturation (or lack thereof) of local communities with richness at continental scales. Rabosky & Hurlburt suggest that local assemblages can be dynamic in diversity as long as there is a zero sum across all communities and through time. But a connection between continental scales and local scales is innate, and understanding how diversity relates over multiple spatial scales is an area of ecological research we need to continue to develop.

Given there are no easy tests of this sort of question (though bacterial microcosm provide some interesting results), we have been forced to draw conclusions based on weak tests and weak evidence. But ecologists do this because this is a truly important question, with huge implications across ecology and evolution. Ecological and evolutionary models make assumptions that implicitly or explicitly about carrying capacity, about determinants of rates of speciation and extinction, about invasion, about why global diversity changes, and these need to be confirmed. Further, if there is a strong ecological feedback of diversity, one of the most important implications is that major perturbations such as extinctions should be followed by major recoveries. In the Anthropocene, that’s an important implication. 


Jeremy Fox said...

Caroline, is the ultimate issue here that the competing hypotheses are too vaguely defined to be testable? I mean, if people are debating whether evidence X even counts as a test of hypothesis Y (as it sounds like they're doing), maybe that means hypothesis Y is too vague to be tractable.

Caroline Tucker said...

I mean, Rabosky and Hurlburt do set out a hypothesis - resource availability limits species richness, and the mechanisms they propose for this are diversity-dependent changes in speciation and extinction rates. I think they would even argue that there are clear predictions that arise from this (lineage speciation rates should decline through time as lineages increase in size, etc).

Whether you consider resource availability -> species richness as too vague to test probably varies depending on what scales you think about/your approach :) As a community ecologist, it seems rather vague, since resources != niches, and we've determined tons of ways for species to partition resources, etc. But I've certainly heard macroecologists suggest that strong tests of this question are possible.

But even if you decide the hypothesis isn't too vague to test, you're right that it probably isn't very tractable. Though I think that's because strong tests are nearly impossible - the data isn't available or can be interpreted in multiple ways, macroevolutionary models are still works in progress, the stochastic component makes hand-wavy-ness too easy...

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