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Book Review

One, two, skip which few? Biodiversity doesn’t always mean ecosystem stability

Moiullot D, Villéger S, Parravicini V, Kulbicki M, Arias-González J, Bender M, Chabanet P, Floeter SR, Friedlander A, Vigliola L and Bellwood DR (2014) Functional over-redundancy and high functional vulnerability in global finish faunas on tropical reefs. PNAS. 111:38. doi: 10.1073/pnas.1317625111

underwearnnotshorts

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It happens to all of us. Three snoozes too late, you drag yourself out of bed into the shower. Make it a cold one, quick and clean. Whew! Record time! But then, you reach into the underwear drawer, and not a single pair is to be found! Your dreaded enemy time has just come face to face with your other nemesis laundry. Whatever shall you do?

(Please don’t tell.)

The classic case of underwear-induced closet collapse is reminiscent of the longstanding ecological idea that biodiversity buffers ecosystems from environmental insults and destructive human activities. Overfish one squid-eating species and another will gladly eat a little more squid to do its part, run out of underwear use a pair of shorts instead. Um, yes.

Uncomfortable yet? You should be. Reeks of controversy!

So, every ecosystem is a closet, and the species are merely clothes in it. If every garment has ten like it, then it should be fairly easy to keep track of when it’s time to do laundry. But, what have we learned so far? You have way more tops than pairs of underwear, and who washes pants anyway? Lose a few shirts and you’ll be fine, but lose a pair of underwear (as happens all the time), and you’re one step closer to impending laundry. Implicit in the idea that biodiversity is nature’s insurance policy is that redundancy is uniform across all species that compose an ecosystem, and, according to a recent study by Mouillot et al. published in PNAS, it isn’t.

To investigate the relationship between species vulnerability and species richness, Mouillot and co-workers surveyed six tropical-reef fish “faunas” across a “nine-fold gradient of species diversity” (i.e., a low of 403 fish species in the Eastern Atlantic, and a high of 3,689 in the Central Indo-Pacific). They categorized fish from 6,316 species into 646 “functional entities” defined by combinations of six unique traits representing the ecological roles played by a particular species and went on to assess functional richness (the functional breadth of a given fauna), functional redundancy (how functional entities are distributed within a fauna), and vulnerability (how deeply affected a given fauna might be by species loss).

To support assumption of a conserved “functional core” across ecosystems, the authors built a “global functional space” encompassing the breadth of all possible combinations of six functional traits. Just as your closet might cover the same functional space as Elton John’s, despite the difference in variety (and necessity) of garments, functional space filled was found to be roughly the same across faunas rich and poor. For example, while the poorest fauna represents only 25 percent of functional entities, it still fills more than half (59 percent) of the functional space defined by all possible combinations of functional traits. Hence, in more species-rich environments, species are “packed” more densely, but the overall ecosystem functions are conserved. To balance it all out, the number of new functional entities that emerges with increased diversity increases at a much slower rate than species richness (roughly one new functional entity for every ten additional species).

Representations of species and functional diversity across six tropical reef fish faunas. Map showing six tropical-reef faunas surveyed. Number of species ranges nine-fold from the most species-rich fauna (Central Indo-Pacific) to the the most species poor fauna (Eastern Atlantic). Histograms for each fauna show number of species (Nb. Sp.), Number of functional entities (Nb. F.E., and functional volume filled by each fauna (Vol. 4d). Below histograms are graphical depictions of the distribution of functional entities in "functional spaces."

One fauna, two fauna, red fauna, blue fauna. Representations of species and functional diversity across six tropical-reef fish faunas. Map shows six tropical-reef faunas surveyed. Number of species ranges nine-fold from the most species-rich fauna (Central Indo-Pacific) to the the most species-poor fauna (Eastern Atlantic). Histograms for each fauna show number of species (Nb. Sp.), Number of functional entities (Nb. F.E.), and functional volume filled by each fauna (Vol. 4d). Below histograms are graphical depictions of the distribution of functional entities in “functional spaces.”

So, if functionality doesn’t increase, where do the “extra species” go? Where do differently colored pairs of underwear end up? Doesn’t matter the color—probably in the underwear drawer. That is, the idea of “functional redundancy” arises as a result of the inability of new species functional groups to keep with a sharp increase in species diversity. Functional redundancy is the number of fish from different species that can be described by the same functional entity. In the most species-rich fauna surveyed, that of the Central Indo-Pacific, functional redundancy averages 7.9 species per functional entity, whereas for the most species-poor fauna, that of the Tropical Eastern Pacific, it averages 2.8 species per functional entity.

The idea of increasing functional redundancy with increasing species richness is old news, but where Mouillot et al. take a turn into uncharted waters is in challenging the notion that this increase in functional redundancy equates to increased robustness to species loss. It’s your birthday, and your multitude of generous friends and family gift you nothing but clothes. Score! No laundry for weeks! Not so fast – only your eccentric aunt gave you a hand-knitted pair of long underwear. The rest gave you mostly shirts and socks.

Relationship between (A) functional richness (B) functional redundancy, (C) functional vulnerability, and (D) functional over-redundancy.

Functional business, to be sure. Relationship between species richness and (A) functional richness, (B) functional redundancy (C) functional vulnerability (D) functional over-redundancy. Note that the gradient of difference collapses from a nine-fold gradient of species richness to a three-fold gradient of functional richness in (A). In (B), the rise in redundancy is much slower than the rise in species-richness, and for (C) and (D), both functional vulnerability and over-redundancy are restricted to a narrow range across all fauna.

Indeed, Mouillot et al. found that, while functional redundancy increases with species diversity, it is disproportionately packed into a small set of functional entities. That is, some functional entities were over-represented, while others were limited to at most a few species. For example, species richness peaks at 222 for the most species-rich functional entities in the Indo-Pacific, while 180 out of 468 functional entities are represented by just one species. Functional vulnerability, the proportion of functional entities represented by only one species, ranges narrowly from 38.5 percent to 54.2 percent across fauna, which is significantly higher than would be expected if species were randomly assigned to functional entities. In other words, in spite of species richness, ecosystems aren’t doing so hot at hedging their bets.

Distribution of functional vulnerability and function-over redundancy for six tropical-reef faunas (colored lines). Both vulnerability and and function over-redundancy fall into a narrow range across all six faunas. The grey lines represent the distribution of functional entities by chance, which predicts lower functional vulnerability and function redundancy than observed.

Feeling vulnerable, not so special. Distribution of functional vulnerability and function-over redundancy for six tropical-reef faunas (colored lines). Species are disproportionately packed into a few functional entities. The grey lines represent the distribution of functional entities by chance, which predicts lower functional vulnerability and function redundancy than observed.

The authors formalize this too-many-eggs-in-one-basket phenomenon by defining the concept of “functional over-redundancy,” which is meant to describe the tendency of a fauna to concentrate redundancy into a few functional entities. They quantify functional over-redundancy as the proportion of species that that occupy functional entities above the average level of functional redundancy. Similar to functional redundancy, they find that functional over-redundancy falls narrowly between 37 percent and 58 percent for all faunas, significantly higher than would be expected by chance. That is, regardless of richness, roughly half of all functional entities in a given fauna are over-represented.

Mouillot et al. conclude their study by testing the “sensitivity” of their results by both eliminating the number of traits used to define functional entities, as well as using a more crude functional characterization. By and large, they find, with the exception of trivial decreases in functional entities, that their results hold for both sensitivity analyses.

Mouillot et al. call a foul on the notion that species richness equates with ecosystem robustness in even the most diverse fish faunas on earth, those of tropical coral reefs. By introducing the concept of the functional over-redundancy, they present a framework that might be extended beyond coral reefs toward understanding the vulnerabilities of other ecosystems. By considering ecosystems by functional organization rather than simply species abundance and diversity, Mouillot et al. present a promising approach for the design of intelligent strategies for managing and restoring ecosystems through identification of functional vulnerabilities in healthy ecosystems, and functional deficiencies in those that are struggling.

The takeaway—in this life you may have too many clothes, but you can never have enough underwear.

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