Friday, July 17, 2015

The first null model war in ecology didn't prevent the second one*

The most exciting advances in science often involve scientific conflict and debate. These can be friendly and cordial exchanges, or they can be acrimonious and personal. Scientists often wed themselves to their ideas and can be quite reluctant to admit that their precious idea was wrong. Students in ecology often learn about some of these classic debates (Clements v. Gleason; Diamond v. Simberloff and Connor), but often other debates fade from our collective memory. Scientific debates are important things to study, they tell us about how scientists function, how they communicate, but more importantly by studying them we are less likely to repeat them! Take for example the debate over species per genus ratios, which happened twice, first in the 1920s, then again in the 1940s. The second debate happened in ignorance of the first, with the same solution being offered!

To understand the importance of testing species-genus ratios we can start with a prediction from Darwin:

As species of the same genus have usually, though by no means invariably, some similarity in habits and constitution, and always in structure, the struggle will generally be more severe between species of the same genus, when they come into competition with each other, than between species of distinct genera (Darwin 1859)

To test this hypotheses, the Swiss botanist, Paul Jaccard (1901) created a ‘generic coefficient’ to describe biogeographical patterns and to measure the effects of competition on diversity. The generic coefficient was a form of the species-genus ratio (S/G), calculated as G/S x 100, and he interpreted a low S/G ratio (or high coefficient) to mean that competition between close relatives was high, and a high ratio (low coefficient) meant that there was a high diversity of ‘ecological conditions’ supporting closely related species in slightly different habitats (Jaccard 1922). At the same time as Jaccard was working on his generic coefficient, the Finnish botanist, Alvar Palmgren, compiled S/G patterns across the Aland Islands and inferred the low S/G values on distant islands to reflect random chance (Palmgren 1921). Over several years, Jaccard and Palmgren had a heated exchange in the literature (across different journals and languages!) about interpreting S/G ratios (e.g., Jaccard 1922, Palmgren 1925). Palmgren’s contention was that the S/G ratios he observed were related to the number of species occurring on the islands –an argument which later work vindicates. A few years after their exchange, another Swiss scientist, Arthur Maillefer, showed that Jaccard’s interpretation was not supported by statistical inference (Maillefer 1928, 1929). Maillefer created what is likely one of the first null model in ecology (Jarvinen 1982). He calculated the expected relationship between Jaccard’s generic coefficient and species richness from ‘chance’ communities that were randomly assembled (Fig. 1 –curve II). Maillefer rightly concluded that since the number of genera increase at a slower rate than richness, the ratio between the two couldn’t be independent of richness.

Jaccard’s generic coefficients plotted by Maillefer showing the relationship between the coefficients (calculated as Genera/Species x 100) and species richness (Maillefer 1929). The four curves depict different scenarios. Curve I shows the maximum values possible, and curve IV is the minimum. Curve III is when coefficients are calculated on sampled values from a flora, which stays on a mean value. Curve II represents the first null model in ecology, where species are randomly sampled (‘hasard’ is translated as chance or luck) and the coefficient was calculated from the random assemblages.

 This example is especially poignant because it foreshadowed another debate 20 years later –and not just in terms of using a null expectation, but that S/G ratios cannot be understood without comparison to the appropriate null. Elton (1946) examined an impressive set of studies to show that small assemblages tended to have low S/G ratios, which he thought indicated competitive interactions. Mirroring the earlier debate, Williams (1947), showed that S/G ratios were not independent of richness and that inferences about competition can only be supported if observed S/G values differed from expected null values. However, the error of inferring competition from S/G ratios without comparing them to null expectations continued into the 1960s (Grant 1966, Moreau 1966), until Dan Simberloff (1970) showed, unambiguously, that, independent of any ecological mechanism, lower S/G are expected on islands with fewer species. Because he compared observationed values to null expectations, Simberloff was able to show that assemblages actually tended to have higher S/G ratios than one would expect by chance (Simberloff 1970). So not only is competition not supported, but the available evidence indicated that perhaps there were more closely related species on islands, which Simberloff took to mean that close relatives prefer the same environments (Simberloff 1970).

Darwin, C. 1859. The origin of the species by means of natural selection. Murray, London.
Elton, C. S. 1946. Competition and the Structure of Ecological Communities. Journal of Animal Ecology 15:54-68.
Grant, P. R. 1966. Ecological Compatibility of Bird Species on Islands. The American Naturalist 100:451-462.
Jaccard, P. 1901. Etude comparative de la distribution florale dans une portion des Alpes et du Jura. Bulletin de la Societe Vaudoise des Sciences Naturelle 37:547-579.
Jaccard, P. 1922. La chorologie selective et sa signification pour la sociologie vegetale. Memoires de la Societe Vaudoise des Sciences Naturelle 2:81-107.
Jarvinen, O. 1982. Species-To-Genus Ratios in Biogeography: A Historical Note. Journal of Biogeography 9:363-370.
Maillefer, A. 1928. Les courbes de Willis: Repar- tition des especes dans les genres de diff6rente etendue. Bulletin de la Societe Vaudoise des Sciences Naturelle 56:617-631.
Maillefer, A. 1929. Le Coefficient générique de P. Jaccard et sa signification. Memoires de la Societe Vaudoise des Sciences Naturelle 3:9-183.
Moreau, R. E. 1966. The bird faunas of Africa and its islands. Academic Press, New York, NY.
Palmgren, A. 1921. Die Entfernung als pflanzengeographischer faktor. Series Acta Societatis pro Fauna et Flora Fennica 49:1-113.
Palmgren, A. 1925. Die Artenzahl als pflanzengeographischer Charakter sowie der Zufall und die säkulare Landhebung als pflanzengeographischer Faktoren. Ein pflanzengeographische Entwurf, basiert auf Material aus dem åländischen Schärenarchipel. Acta Botanica Fennica 1:1-143.
Simberloff, D. S. 1970. Taxonomic Diversity of Island Biotas. Evolution 24:23-47.
Williams, C. B. 1947. The Generic Relations of Species in Small Ecological Communities. Journal of Animal Ecology 16:11-18.

*This text has been modified from a forthcoming book on ecophylogenetics authored by Cadotte and Davies and published by Princeton University Press

Wednesday, July 8, 2015

Taking stock of exotic species in the new wild: Acknowledging the good and the bad.*

Are exotics good or bad? They are neither. They just are. But some exotics cause harm and impede certain priorities, and debates about exotics often ignore reality.

Book review: Fred Pearce. 2015. The New Wild: Why Invasive Species Will Be Nature’s Salvation. Beacon Press

There has been much soul-searching in invasion biology, with attacks, and subsequent rebuttals, on the very nature of why we study, manage and attempt prevent the spread of exotic species (Davis et al. 2011) (Alyokhin 2011, Lockwood et al. 2011, Simberloff 2011). What is needed at this juncture is a thoughtful and balanced perspective on the nature of the discipline of biological invasion. Unfortunately, the book “The New Wild” authored by Fred Pearce, is not that balanced treatment. What is presented in this book is a very one-sided view, where counter-evidence to the thesis that exotics will save nature is most often overlooked, straw men are erected to aid in this goal, and the positions of working ecologists and conservation biologists are represented as simplistic, anachronistic or just plain incorrect.

What Pearce has written is a book-long argument about why exotics shouldn’t be feared, but rather embraced as a partial solution to anthropogenic land use change. I do not wish to undermine the reality that exotics can play important roles in urban landscapes, or that some ecologists and conservation biologists do indeed harbour suspicions of exotics and subscribe to unrealistic notions of purely native landscapes. Exotic policy is at the confluence of culture, science, economics and politics, and this is why the science is so valuable (Sandiford et al. 2014). For Pearce, the truth of what most ecologists do and think seems like an inconvenient reality.  There are a number of pervasive, frustrating problems with Pearce’s book, where bad arguments, logical flaws and empirical slight-of-hand obfuscate issues that desperately need honest and reflective treatment.

A monoculture of the exotic plant Vincetoxicum rossicum that spans open and understory habitats near Toronto, Canada (photo by M. Cadotte). This is a species that interferes with other management goals and needs to be actively managed.

There are major problems with ‘The New Wild’ and these include:

1) A premise built on a non sequitur and wishful thinking. The general premise of the book, that exotics represent a way out of our environmental doldrums, is myopic. Pearce’s reasoning seems to be that he has conflated “the world is not pristine and restoration is difficult…” with the alternative being that exotics are positive and “we should bring them on”. Certainly we can question exotic control efficacy, costs and conservation goals, but that does not mean that exotics are necessarily the solution.

      2)   Underrepresenting the observed effects of some invasive non-indigenous species. Pearce’s book is not balanced. The perceived benefits of exotics in this ‘New Wild’ are extolled while dismissing some of the problems that invasive ones might cause. He says that exotics typically “die out or settle down and become model eco-citizens” (p. xii). But there is a third outcome that Pearce ignores –they move in and become unruly neighbours. When he must acknowledge extinctions, he minimizes their importance. For example when discussing Hawaiian bird extinctions: “The are only 71 known extinctions” (p. 12 –italics mine), or with California: “But only 30 native species are known to have become extinct as a result [of exotics]” (p. 64 –italics mine).

He also implies throughout the book that exotics increase diversity because “Aliens may find new jobs to do or share jobs with natives.” (p. 113). The available evidence strongly suggests that the numbers of species inhabiting communities has not increased over time (Vellend et al. 2013, Dornelas et al. 2014). Which on the surface seems like a good thing, except that many communities are now comprised of 20-35% exotics. This means that there have been losers. Vellend and colleagues (2013) show that the largest impact on native species diversity has been the presence of exotics. So, they do not necessarily find new jobs, but rather outcompete some natives.

      3)   Conservation biologists and ecologists in the crosshairs. Pearce continually lauds those like-minded, outspoken advocates of exotics while belittling ecologists and conservation biologists who don’t agree with him. His disrespect for the process of science comes in two forms. First, he seldom considers evidence or presents opinions counter to his thesis. He gives a partial reason about this bias; he says that ecologists (except for those few brave pioneering souls) ignore novel ecosystems and the functional contributions of exotics (for example on p. 13). This is demonstrably false (see next section). Pearce has little affection for conservation biologists and mainstream ecologists. Both groups are disparaged and dismissed throughout the book. Conservation biologists get a particularly rough ride, and he never acknowledges the difficulty of their task of balancing multiple priorities: extinction vs. ecosystem function, habitat preservation vs. socioeconomic wellbeing, etc. For example, Pearce states: “Conservation scientists are mostly blind to nature outside of what they think of as pristine habitats and routinely ignore its value” –again a demonstrably false assertion.

In a particularly galling example, Pearce resorts to ‘guilt by association’ as an ad hominem attack to undermine the validity of opposing views. He links conservation with eugenics: “Many conservationists of the first half of the twentieth century were prominent proponents of eugenics” (p. 141). It would be equally valid to state that most journalists were proponents of eugenics in the first half of the twentieth century. Pearce, being a journalist, should see this as a specious argument at best.

Ecologists share in this odd and unfair derision. “Ecologists are tying themselves in knots because they refuse to recognize that these novel, hybrid ecosystems are desirable habitats for anything.” (p. 156). Unfortunately for Pearce, there are more than 4000 papers on ‘novel ecosystems’.

      4)   Misrepresenting modern ecology and conservation. Pearce attacks ecological science throughout the book and as an example Pearce makes observations about the role of disturbance and refusal to acknowledge this by ecologists “intent on preserving their own vision of balanced nature” (p. 144). However, disturbance has been a central component of community ecology for the past five decades. Because of this balance-of-nature view, Pearce says ecologists are not studying degraded, disturbed or recovering systems. For example, with secondary forests, he says: “Yet the blinkered thinking persists. Degraded forests and forests in recovery are almost everywhere under-researched and undervalued.” (p. 157). Yet there are almost 9,500 papers on secondary forests –highlighting the ecological interest in these widespread systems. There are numerous such examples.

      5)   A black and white, either-or dichotomy.  What Pearce provides is a series of stark dichotomies with little room for subtle distinction. He ties resilience and ecosystem wellbeing to the arrival of exotics, without adequately assessing the drawbacks: “Nature’s resilience is increasingly expressed in the strength and colonizing abilities of alien species …we need to stand back and applaud” (p. xii).

Invariably in ecology, debates over ‘either/or’ dichotomies end up with the realization that these dichotomies are endpoints of a continuum. This is exactly the case with exotics. Are they bad or good? The answer is neither. They just are. Some exotics species provide economic opportunity, ecosystem services and help meet other management goals. Some exotics cause harm and impede certain priorities. Modern management needs to be, and in many cases is, cognizant of these realities.

Alyokhin, A. 2011. Non-natives: put biodiversity at risk. Nature 475:36-36.
Davis, M. A., M. K. Chew, R. J. Hobbs, A. E. Lugo, J. J. Ewel, G. J. Vermeij, J. H. Brown, M. L. Rosenzweig, M. R. Gardener, and S. P. Carroll. 2011. Don't judge species on their origins. Nature 474:153-154.
Dornelas, M., N. J. Gotelli, B. McGill, H. Shimadzu, F. Moyes, C. Sievers, and A. E. Magurran. 2014. Assemblage Time Series Reveal Biodiversity Change but Not Systematic Loss. Science 344:296-299.
Lockwood, J. L., M. F. Hoopes, and M. P. Marchetti. 2011. Non-natives: plusses of invasion ecology. Nature 475:36-36.
Sandiford, G., R. P. Keller, and M. Cadotte. 2014. Final Thoughts: Nature and Human Nature. Invasive Species in a Globalized World: Ecological, Social, and Legal Perspectives on Policy:381.
Simberloff, D. 2011. Non-natives: 141 scientists object. Nature 475:36-36.
Vellend, M., L. Baeten, I. H. Myers-Smith, S. C. Elmendorf, R. Beauséjour, C. D. Brown, P. De Frenne, K. Verheyen, and S. Wipf. 2013. Global meta-analysis reveals no net change in local-scale plant biodiversity over time. Proceedings of the National Academy of Sciences 110:19456-19459.

 *This post is a synopsis of my book review in press at Biological Invasions