Hypothesis testing, curve fitting, and data mining in macroecology

Nicholas J. Gotelli
Department of Biology, University of Vermont.
e-mail: Nicholas.Gotelli(at)uvm.edu

Changes in technology and methodology can have a big influence on how we do science. In this essay, I will discuss how new methods for the acquisition and analysis of data have affected biogeography and macroecology.

The underlying data used by macroecologists are geo-referenced specimen collections (GBIF 2008). For many decades, biogeographers explored the globe to collect and catalog these kinds of data (e.g. Darlington 1957). The numbers, usually counts of species or maps of geographic ranges, were plotted in simple graphs and used in support of narrative explanations and historical accounts of the patterns. Explicit hypothesis-testing was rare, although pioneering analyses of taxonomic diversity indices by C.B. Williams and other European ecologists (Järvinen 1982) foreshadowed the statistical perspective that would begin to dominate ecology and biogeography in the 1970s (Gotelli and Graves 1996).

Today, the widespread availability of compiled data sets on the internet means that young scientists can begin successful careers in macroecology without ever going in the field to collect data themselves. Of course, since most of the earth’s biota has not even been described taxonomically (May 1995) – much less mapped biogeographically – there is still a great deal of primary data collecting to do. But even some of this activity may become automated, with the most promising avenue being the mapping of vegetation through the use of remote sensing and satellite imagery (Gillespie et al. 2008).

With less emphasis on data collection, more energy has gone into statistical analysis and interpretation. Sophisticated methods such as spatial regression analysis (Lichstein et al. 2002) have been used to compare patterns in multiple data sets and address long-standing hypotheses about the origin and maintenance of the latitudinal gradient in species richness (Rohde 1992, Willig et al. 2003). An entire subdiscipline of bioclimatic niche modeling has emerged as macroecologists have used species occurrence data to predict how biotas will respond to global climate change (Elith et al. 2006).

In spite of this statistical sophistication, macroecologists still have not achieved a satisfactory understanding of global patterns of species diversity (Currie et al. 2004), nor have they developed trustworthy tools for forecasting future biotic change (Araújo and Rahbek 2006). In fact, the published conclusions still sound an awful lot like the narratives of the early biogeographers! But instead of making these arguments on the basis of simple species richness plots, macroecologists make them on the size of the p-values or the correlation coefficients from their regression models.

There are two related problems here, one with the hypotheses and the other with the statistical methods. For the most part, hypotheses in macroecology are just verbal descriptions of mechanisms (“higher productivity in the tropics allows for more biodiversity”). But since multiple explanations can generate the same qualitative patterns (“greater temperature stability in the tropics allows for more biodiversity”), we are not going to easily distinguish these mechanisms through qualitative assessment of correlations alone.

In this regard, I think the most important recent breakthrough in macroecology has been the development of metabolic theory (Allen et al. 2002). This theory, derived from first principles that do not depend in a circular way on existing data, predicts a quantitative relationship between temperature and biodiversity. Instead of just testing a null hypothesis of a slope of zero, we can now test whether observed slopes (with appropriate transformations) deviate from -0.65, the predicted value from the model (Hawkins et al. 2007). Controversy over the empirical support for metabolic theory (Hawkins et al. 2007, Gillooly and Allen 2007) should not obscure its importance: metabolic theory makes quantitative, not just qualitative, predictions and that is what we need right now in macroecology.

Theoreticians should step up to the plate and develop quantitative theories for other hypotheses in macroecology. As recently proposed by O’Brien (2006), the water-energy model may provide an emerging framework that will generate functional forms for water and energy variables derived from first principles of physiology and physical constraints imposed by the energetics of liquid water. For now, however, these models are either entirely verbal (Vetaas 2006), or they are derived from fitted regression functions that are specific to particular taxa, spatial scales, and continents (O’Brien 1998).

In addition to the development of new theory, we need to move beyond analytical methods that simply fit curves to data and test patterns against simple statistical null hypotheses. Some macroecologists are beginning to develop stochastic simulation models that include explicit algorithms for the origin, spread, and extinction of species in a bounded geographic domain (e.g. Storch et al. 2006, Rahbek et al. 2007, Rangel et al. 2007) These mechanistic simulation models (Grimm et al. 2005) have their roots in the mid-domain effect (Colwell and Lees 2000), a pleasingly simple explanation for species richness gradients that emerged from the random placement of contiguous species ranges in a bounded domain. This kind of modeling exercise raises its own challenges: how do we empirically estimate model parameters, and how do we explore the behavior of such a model over a potentially very large parameter space? But this simulation approach may allow macroecology to move beyond statistical correlations, and can serve as a nice complement to theoretical investigations. Simulation models may even provide quantitative predictions in cases where the mathematical models do not have a tractable analytic solution.

In a provocative essay in Wired magazine, Anderson (2008) speculates that one day traditional hypothesis testing will be unnecessary. Some data-mining enthusiasts believe that, with enough data, correlations will reveal mechanisms in comprehensive statistical models that encompass all possible data. I think the data miners are probably right. Exciting new work in computer science has led to very sophisticated “reverse-engineering” algorithms that have great promise for uncovering the functional form of relationships among correlated variables. These new iterative methods use data partitioning, automated probing, and snipping to sequentially modify and test underlying nonlinear functions with data-rich time series.

For example, Bongaard and Lipson (2007) successfully recovered the functional form of the movement of a pendulum using as input the temporal series of spatial coordinates of a swinging pendulum. Their algorithm repeatedly “sampled” the data set from the most critical regions (where the pendulum was changing direction) and iteratively arrived successfully at the correct equations for motion.

Interestingly, the same methods were not so successful when applied to the famous ecological time series of snowshoe hare and Canadian lynx populations (Elton and Nicholson 1942). The algorithm did generate a pair of coupled differential equations (Bongaard and Lipson 2007). However, we know that the hare-lynx cycle is not caused entirely by coupled predator-prey interactions.

The problem, of course, is not the algorithm, but the limited data that it was fed. The time series of pelt records from the Hudson Bay Company does not reveal the critical observations of hare populations on islands in eastern Canada that cycle in the absence of the lynx (Keith 1963). The analysis also did not include time series on the secondary plant compounds in tundra vegetation, which accumulate under intense grazing and may be ultimately responsible for endogenous cycles of the hare (Keith 1983). And the model did not include time-series on snowpack depth or solar sunspot activity, both of which probably contribute to the regional synchrony of hare lynx cycles (Sinclair et al. 1993).

Without such “expert knowledge” it is easy to understand why the model failed. If those data inputs were provided, I think it is very likely the model would reveal the correct functional form of the relationships among hare, lynx, vegetation, and climate. But for now, the use of passive machine-learning algorithms applied to large data sets is an inefficient way to test hypotheses and make progress in macroecology. And given the pressing need to understand how biotas will respond to climate change, I am not sure we have the luxury of waiting for these comprehensive data sets to accumulate.

Nevertheless, the paradigm of machine learning seems to be the direction that much of the bioclimatic niche modeling research is going. If the goal of this research is to understand how biotas will shift in response to climate change, I think it is going to be much more fruitful if we combine it with an experimental approach. Experimental translocation of individuals beyond their current range boundaries (Hellmann et al. 2008) and experimental manipulations of abiotic variables to mimic effects of climate change on populations and communities (Harte and Shaw 1995, Suttle et al. 1997) are very powerful approaches. Experiments can provide realistic parameter estimates for bioclimatic niche models. Even simple models that are supported by experimental data will probably be more trustworthy than sophisticated models that are not.

In sum, the availability of large data bases, the emergence of quantitative predictive theories, and the development of new computational tools and simulation methods make this an exciting time to be studying macroecology. There are pressing applied problems of global climate change that we can address with these new tools and data. And along the way, perhaps we will even answer some unresolved questions in biogeography about species richness gradients.

Acknowledgements
This essay was inspired by the work of the Synthetic Macroecological Models of Species Diversity Working Group supported by the National Center for Ecological Analysis and Synthesis, a Center funded by NSF (Grant #DEB-0553768), the University of California, Santa Barbara, and the State of California.

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Do microorganisms have biogeography?

Diego Fontaneto
Imperial College London, Division of Biology, Silwood Park
e-mail: d.fontaneto(at)imperial.ac.uk
Joaquín Hortal
NERC Centre for Population Biology, Imperial College London, Silwood Park
e-mail: j.hortal(at)imperial.ac.uk

Diego Fontaneto (right) and Joaquín Hortal (left)

Zoologists and botanists look to exotic places in order to find interesting new species and higher taxa. Over the last few centuries, scientific expeditions in remote places have indeed discovered new species and even higher taxa of limited distribution. Such discoveries still occur in recent years. The new insect order Mantophasmatodea in Namibia and Tanzania (Klass et al., 2002) was only known from fossil specimens in amber (Arillo et al., 1997). Even recently the new rodent species Laonastes aenigmamus was found in Laos; a new family was proposed to classify this species (Laonastidae; Jenkins et al., 2004), although it was later included in the Diatomydae (Dawson et al., 2006), a family that was also known only from fossil remnants (Mein & Ginsburg, 1997). The fact that in both cases these new higher taxa were already known from fossils does not diminish the need to explore remote areas to find new living branches in the macroscopic part of the tree of life.

Hypsibius dujardini (phylum Tardigrada).
Picture by Willow Gabriel and Bob Goldstein / Public Domain. Source: http://tardigrades.bio.unc.edu/.

In contrast, collecting samples in remote areas, scientists working on the less-known microscopic organisms (smaller than 2mm) invariably found species and higher taxa that could be ascribed to taxa already known from Europe (Fenchel & Finlay, 2003). Once completely new higher taxa are discovered, they are quickly found to be widely distributed. The recently described microscopic animal phyla, Loricifera from marine sediments off the coast of France (Kristensen, 1983), Cycliophora on the mouthparts of lobsters in Denmark (Funch & Kristensen, 1995) and Micrognathozoa in cold springs in Antarctica (Kristensen & Funch, 2000), have all been suddenly found in regions very distant from the original type locality, but in similar habitats, which were in fact previously unexplored (Todaro & Kristensen, 1998; De Smet, 2002; Nedved, 2004).
The difference between macro- and microorganisms can be illustrated with the example of what is actually found when a small region is surveyed. Forty-eight Tardigrada species were found in an extensive survey of rock mosses and leaf litter of a mountain range at the Iberian Peninsula (using tiny 3x3 cm cores) (Guil, 2008). From these, only six species (12.5%) are only known from a single continent (Europe). This count includes two new species that, obviously, are only known from Central Iberian Peninsula. At least for now. Taxonomical and biogeographical knowledge on the phylum Tardigrada is far from being complete, and is seriously unbalanced through the regions of the world (Guil & Cabrero-Sañudo, 2007). However, this example illustrates that the communities of microscopic organisms host high proportions of widespread and cosmopolitan species, to the extent that 20% of all known bdelloid rotifers have been found in a small Italian valley (Fontaneto et al., 2006), and 50 % of all named species of heterotrophic flagellates have been recorded in a small Danish Bay (Fenchel and Finlay, 2004).
It is commonly thought that most species have restricted distributions (see, e.g., Gaston, 2003). However, very few microbiologists will endorse such a statement (see, e.g., Fenchel & Finlay, 2003, 2004). Why do microscopic and macroscopic organisms differ so widely in their patterns of distribution? The Baas-Becking (1934)’s hypothesis, also known as the “Everything is Everywhere” (EisE) hypothesis, encapsulates the classical view that microscopic organisms are globally distributed due to their high potential for dispersal (Kellogg & Griffin, 2006). Small size and an ability to enter dormancy, and therefore to produce dormant propagules (Cáceres, 1997; Bohonak & Jenkins, 2003; Fenchel & Finlay, 2004), might explain why prokaryotes and some microscopic eukaryotes, such as protists and small invertebrates, have acquired global distributions.
The assumption that organisms smaller than 2mm have cosmopolitan distribution often holds true when species are defined using traditional taxonomy. However, the EisE hypothesis has been challenged recently. Recent molecular evidence reveals distance-decays in the similarity of microorganisms belonging to the same traditional species in a variety of microscopic organisms, including prokaryotes (Cho & Tiedje, 2000; Whitaker et al., 2003), protists (Darling et al., 2004; Foissner, 2006; Telford et al., 2006), and fungi (Taylor et al., 2006). Other studies have found cases of restricted distributions solely by re-evaluating morphological evidence within species previously assumed to have cosmopolitan distributions (Smith & Wilkinson, 2007). All this evidence points out that there might be a high degree of cryptic diversity in the microbial world, and that there are more restrictions to the dispersal of microscopic organisms than previously thought.

Chaetonotus sp. (phylum Gastrotricha).
Picture by M.A.Todaro. Source: http://www.gastrotricha.unimore.it/

The current debate on the EisE hypothesis divides scientists in two major groups (Whitfield, 2005). On one side, scientists following the EisE hypothesis in its original form assume that species differences in samples from different areas occur because of environmental differences, and not because of restricted dispersal. Thus, they consider that “everything is everywhere, but the environment selects” is the rule for microorganisms (e.g. de Wit & Bouvier, 2006; Fenchel & Finlay, 2006). On the opposite position, other scientists propose that classical morphological taxonomy of microscopic organisms is not able to resolve their actual diversity, and therefore that cosmopolitan ranges result from misidentification and lumping of spatially isolated lineages (e.g. Coleman, 2002; Foissner, 2006; Taylor et al., 2006).
The straightforward way of solving this debate would be to determine if environmental selection by microorganisms (i.e., environmental filtering) does actually cause reproductive isolation and/or limits gene flux. It has been argued that it would be difficult to falsify the EisE+environmental selection hypothesis, because there could be unmeasured aspects of the environment that differ consistently among regions (Foissner, 2006). However, if we assume a dense sample of equivalent habitats across sampling regions, the hypothesis makes clear predictions about genotype distributions. If EisE is the rule, the degree of genetic relatedness between two individuals should be independent of the geographic distance between them, except that individuals within a habitat patch might be more closely related to one another than those in different habitat patches. Conversely, if EisE does not hold true, spatially explicit models should work in the same way as they do for macroorganisms, and genetic diversity should be related to geographic distances by a classical distance-decay relationship.
Microscopic animals can be used as a model to test the EisE hypothesis, to assess (i) if there are environmental effects on the distribution and composition of microscopic assemblages, and (ii) if there are environmentally- or distance-driven genetic differences among the individuals of the same evolutionary entity (i.e., the same taxon). On the one hand, environmental effects on microscopic communities across space have been tested in very few model organisms; up to now empirical studies are available only for local samples for bdelloid rotifers (Fontaneto et al., 2006), tardigrades (Guil et al., conditionally accepted), and mites (Valdecasas et al., 2006). These studies show contrasting results. While habitat filtering seems to be important at the landscape scale for bdelloid rotifers and tardigrades, water mites show only weak associations with habitat. On the other hand, explicit genetic tests on the strength of spatial patterns (such as distance-decay relationships) have been performed only for two genera of bdelloid rotifers (Fontaneto et al., 2008), and for one species complex of monogonont rotifer(Brachionus manjavacas; Gómez et al., 2007; Mills et al., 2007). These studies confirmed that even microscopic animals have biogeographies and show persistent genetic signature of colonisation.
Undoubtedly, more studies on the diversity patterns of microorganisms, dispersal abilities and their phylogeographic structure are yet needed (Jenkins et al., 2007). Supporting or denying the EisE hypothesis needs much more work at different spatial scales, and also a comprehensive coverage of other groups of microscopic organisms, including bacteria, protists, microscopic algae, animals and fungi. However, the potential of microorganisms for biogeography and macroecology might go far beyond than merely solving the question of whether they are truly widespread, or not. As said before, we know that at least a few groups show responses to microenvironmental differences, which sometimes can be very narrow. Little is known about the exact nature of these responses, but identifying the particular responses of individual species provides a way of tracking environmental changes by comparing the composition of microbial assemblages. This, together with ubiquity of some microscropic groups, makes them potential candidates to be used as universal indicators, allowing comparisons between very distant places distributed worldwide.

The monogonont rotifer Brachionus manjavacas.
Picture by Diego Fontaneto and Giulio Melone

Apart from that, microhabitats in nature provide means of testing biogeographical hypotheses, as exemplified by the analysis of the species-area relationship carried out by Bell et al. (2005). They assumed that water-filled holes at the base of large beech trees are independent islands sharing the same bacterial species pool, and measured species richness as bacterial genetic diversity, and island size as water volume in each tree-hole. The species area relationship (measured as a power law) was highly significant, and showed a slope similar to the one found in many macroscopic continental island systems. This is just an example of the silent revolution undergoing in microbial ecology (Prosser et al., 2007). Microbial model systems are already being used to re-analyze part of the current theoretical body of ecology and biogeography (Jessup et al., 2004), which until recently have been almost exclusively based on macroscopic organisms.
A better knowledge on the biology of some groups of microorganisms and the molecular techniques now available can help solving two of the major drawbacks of biogeography as a hard science: the impossibility or extreme difficulty of performing experiments, and the limited number of real world examples that can be used to evaluate the proposed hypotheses and/or models. Contingency makes the evaluation of concurrent hypotheses on the distribution of biodiversity very difficult (see, e.g., Hawkins, 2008). We believe that some microorganisms provide a mean to make true experiments in biogeography, for they allow setting up experimental designs affordable in terms of time and money. For example, being the dispersal of some of them potentially unlimited and passive at the same time, they can allow formal tests of the neutral theory (Hubbell, 2001). By adding filters to dispersal and/or designing experimental islands with particular characteristics, experiments on island biogeography can also be made. Some groups, such as bacteria, or the bdelloid rotifers, tardigrades and mites mentioned above, can provide manageable study systems and help establish the basis of a harder biogeographical science.

The bdelloid rotifer Macrotrachela quadricornifera.
Picture by Diego Fontaneto and Giulio Melone.

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Recent progress toward understanding the global diversity gradient

Bradford A. Hawkins
Department of Ecology & Evolutionary Biology, University of California, Irvine
e-mail: bhawkins(at)uci.edu

Four years ago I published a guest editorial opining that we are making rapid progress toward understanding global patterns of diversity (Hawkins 2004). I also claimed that we still did not have a complete answer, because although the evidence that climate strongly influences the distributions of currently existing species is solid, there was little consensus about the mechanisms driving patterns over evolutionary time. Even so, the increasing availability of the right sort of data coupled with modern phylogenetic methods has us well on the way to finding the solution to the oldest problem in ecology and biogeography, and several important papers have appeared in the past four years. Although none of these provide incontrovertible evidence as to the final answer, in guest editorials the rules of evidence are more relaxed and one can make an argument without the formality that is required in a peer-reviewed article. Based on these rules, and hoping that taking a strong position in an informal setting might stimulate debate, I suggest that we now have sufficient evidence to conclude that niche conservatism and time for speciation are the primary drivers of the contemporary diversity gradient. And while it remains true that additional data on geographic variation in speciation/extinction rates and the strength of biotic interactions are needed, these appear to be secondary effects that do not need to be invoked to explain the general patterns we see; that is to say, they are details, and any differences we may find in these processes will not change the overall explanation for why the tropics have more species. Clearly, this is a strong opinion, so on what basis can I claim that we know the answer? Although a large number of papers have been published on this topic, three recent ones stand out as critical pieces of the puzzle: Wiens & Donoghue (2004), Currie et al. (2004) and Mittelbach et al. (2007).

Although the idea of niche conservatism did not originate with Wiens & Donoghue (2004), this short paper reminded many ecologists of its existence and succinctly described a potentially powerful explanation for higher tropical diversity, based on three sets of observations: (1) most very rich tropical groups originated there (giving them more time to speciate), (2) the world’s climates were mostly ‘tropical’ until the Oligocene (providing a very large area for new clades to arise and subsequent radiations to occur), and (3) it has been difficult for species adapted to tropical climates to break into the younger, cool temperate zones (tropical niches are conserved over long time periods in many clades). Once these three tenets are accepted, higher tropical diversity is not only expected, it is virtually guaranteed. Numerous papers testing this idea have appeared in recent years (see Mittelbach et al. 2007), and the power of niche conservatism to explain diversity patterns at a range of spatial scales is rapidly becoming evident. It is notable that most of the papers in the recent special feature of The American Naturalist on evolutionary approaches to understanding diversity patterns discuss or test this (Harrison & Cornell 2007, Harrison & Grace 2007, Hawkins et al. 2007a, Roy & Goldberg 2007, Wiens 2007). One powerful aspect of niche conservatism is that it predicts diversity patterns based on the climatic conditions where (and perhaps when) groups arose and began radiating, and when niche conservatism is coupled with time for speciation it is also able to explain why some groups are more diverse in cool climates than in warm ones (i.e., it explains exceptions to the general ‘latitudinal gradient’ as well as when it will exist). All in all, this is a potent hypothesis and is the one to beat, although one would have to be very brave indeed to claim that a single hypothesis can explain everything on both land and sea.

Global amphibian species richness gradient (map extracted from the Global Amphibian Assessment; IUCN, Conservation International, and NatureServe, 2006; original data available at http://www.globalamphibians.org/)

The second piece of the puzzle comes from Currie et al. (2004), although it mostly reports negative results rather than positive ones. The primary alternatives to historical hypotheses have been based on the often strong correlations between current climatic conditions and diversity, and there is no need to dwell on the debates in the literature over the past 20 years as to whether understanding richness gradients requires knowledge of the past or not. What Currie et al. (2004) showed was that predictions arising from hypotheses based on current climates (the ‘more individuals’ hypothesis and a dispersal based version of the ‘physiological tolerance’ hypothesis) are not well supported by the evidence. Another recent theory proposing that current temperature patterns explain diversity gradients, the metabolic theory of ecology (see Allen et al. 2002), is also not supported by empirical evidence (Hawkins et al. 2007b). So, if the evidence is to be believed, one has to concede that history does matter after all, which allows us to stop arguing about ‘if’ and start focusing on ‘how’. Although many previous papers dating back over 100 years have argued for the importance of history, many workers feel that rejecting hypotheses using empirical tests carries more weight than logical argument, so Currie et al.’s explicit tests represent real progress in my opinion. This paper also conducted a test, in so far as was possible, of one of the major evolutionary alternatives to niche conservatism and time for speciation, which they called the ‘speciation rate’ hypothesis, which proposes that tropical diversity is high due to accelerated speciation rates driven by climate. They found that tests were few, and the results were mixed. But this also set the stage for the third key paper, Mittelbach et al. (2007).

Although a review paper rather than a research paper, Mittelbach and an illustrious set of co-authors provide a thorough evaluation of the state of the field and lay out the issues involved very well. Indeed, this paper is required reading for anyone seriously interested in understanding the global diversity gradient. However, in the spirit of generating debate, one does not have to agree with all of their conclusions about the relative importance of particular evolutionary mechanisms. Not surprisingly, they see two general processes as possibly being important: time for speciation (which I would argue is a stronger explanation when coupled with niche conservatism), or higher diversification rates in the tropics, acting through either greater speciation or lower extinction. With respect to time for speciation, given the three tenets presented in Wiens & Donoghue (2004), greater tropical diversity is inevitable unless one is willing to accept some very unlikely scenarios. That is, the global diversity gradient would exist irrespective of spatial variation in speciation rates unless the latter were impossibly high in the temperate zones. If this is true, then arguments about relative diversification rates are really arguments about the magnitude of slopes of richness vs. environment regressions and not about the sign of the slopes.

Another telling point about the studies included in Mittelbach et al.’s review is that even if we ignore the serious difficulty in partitioning diversification rates into its components (which greatly reduces our ability to interpret such analyses), the results obtained so far have been mixed, as also reported by Currie et al. (2004). In some cases workers are finding faster net diversification, speciation or extinction rates in the tropics, sometimes they find the opposite, and sometimes there is no spatial pattern at all. But if increased tropical speciation rates are indeed the explanation for higher tropical diversity, the signal should be clear and consistent among groups. The fact that it is not suggests that it is not a strong or universal process and so must be secondary to some other dominating driving effect. Therefore, although Mittelbach et al.’s evaluation of the evidence is measured and gives all sides of the argument equal weight, a case could be made that time for speciation will ultimately prove to explain much more spatial variation in richness than variable speciation rates. Of course this does not mean that we should ignore the latter issue, as there are many reasons to understand how the speciation process varies in time and space. As an aside, speciation rates in the tropics may actually be greatest in mountains (see e.g. Kozak & Wiens 2007), which raises some interesting questions about if they are more strongly influenced by the strength of local climatic gradients than by warm climates per se.

It is also probably the case that geographic variation in extinction rates is relatively more important than variable speciation rates, but extinction can largely be interpreted as a effect of niche conservatism in the face of climate change (see e.g. Hawkins et al. 2007a). And climate change also provides a pressing reason for studying extinction rates, since they appear to be on the rise. Irrespective, as far as understanding why Brazil supports more species than Alaska, niche conservatism in the face of global climate change since the Tertiary probably explains the bulk of the difference (and even further back for very old taxonomic groups). But we should not forget that climate patterns over ecological time spans matter as well; the Sahara is not depauperate because of history alone, but because all life requires access to water one way or another and this is as true today as it was in the past. The biotic responses to rapid climate change we are documenting now are evidence enough that contemporary events influence diversity. Although not everyone may agree about what aspect of the past ultimately drives diversity, no one denies that species have limited abilities to adapt to or track changing climatic conditions. These limitations extended over entire clades evolving over long time periods can also provide a parsimonious explanation for global patterns of diversity. Although the debate continues, at the current rate of progress we should be able to reach a consensus soon.

References
Allen, A. P., Gillooly J. F. & Brown, J. H. (2002) Global biodiversity, biochemical kinetics, and the energetic-equivalence rule. Science 297, 1545-1548.
Currie, D. J., Mittelbach, G. G., Cornell, H. V., Field, R., Guégan, J.-F., Hawkins, B. A., Kaufman, D. M., Kerr, J. T., Oberdorff, T., O’Brien, E. M., & Turner, J. R. G. (2004) Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. Ecology Letters, 7, 1121-1134.
Harrison, S. P. & Cornell, H. V. (2007) Introduction: merging evolutionary and ecological approaches to understanding geographic gradients in species richness. The American Naturalist, 170, S1-S4.
Harrison, S. P., & Grace, J. B. (2007) Biogeographic Affinity helps explain productivity-richness relationships at regional and local scales. The American Naturalist, 170, S5-S15.
Hawkins, B. A. (2004) Are we making progress toward understanding the global diversity gradient? Basic and Applied Ecology, 5, 1-3.
Hawkins, B. A., Diniz-Filho, J. A. F., Jaramillo, C. A., & Soeller, S. A. (2007a) Climate, niche conservatism, and the global bird diversity gradient. The American Naturalist, 170, S16-S27.
Hawkins, B. A., Albuquerque, F. S., Araújo, M. B., Beck, J., Bini, L. M., Cabrero-Sañudo, F. J., Castro Parga, I., Diniz-Filho, J. A. F., Ferrer-Castán, D., Field, R., Gómez, J. F., Hortal, J., Kerr, J. T., Kitching, I. J., León-Cortés, J. L., Lobo, J. M., Montoya, D., Moreno, J. C., Olalla-Tárraga, M. Á., Pausas, J. G., Qian, H., Rahbek, C., Rodríguez, M. Á., Sanders, N. J. & Williams, P. (2007b) A global evaluation of metabolic theory as an explanation for terrestrial species richness gradients. Ecology, 88, 1877-1888.
Kozak, K. H. & Wiens, J. J. (2007) Climatic zonation drives latitudinal variation in speciation mechanisms. Proceedings of the Royal Society of London B, 274, 2995-3003.
Mittelbach, G. G., Schemske, D. W., Cornell, H. V., Allen, A. P., Brown, J. M., Bush, M. B., Harrison, S. P., Hurlbert, A. H., Knowlton, N., Lessios, H. A., McCain, C. M., McCune, A. R., McDade, L. A., McPeek, M. A., Near, T. J., Price, T. D., Ricklefs, R. E., Roy, K., Sax, D. F., Schluter, D., Sobel, J. M., & Turelli, M. (2007) Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecology Letters, 10, 315-331.
Roy, K. & Goldberg, E. E. (2007) Origination, Extinction, and Dispersal: Integrative Models for understanding present-day diversity gradients. The American Naturalist, 170, S71-S85.
Wiens, J. J. (2007) Global patterns of diversification and species richness in amphibians. The American Naturalist, 170, S86-S106.
Wiens, J. J., & Donoghue, M. J. (2004) Historical biogeography, ecology and species richness. Trends in Ecology and Evolution, 19, 639-644.

Christen Raunkiær – one of several early island biogeographers

Henning Adsersen
Center for Macroecology, Institute of Biology, University of Copenhagen
e-mail: adser(at)bi.ku.dk


Islands, especially isolated oceanic islands, have always held a fascination for me, both emotionally and intellectually. Likewise they have fascinated travelers ever since the first oversea transportation means were invented and employed. This fascination and fantasy created early a fertile substrate for tales, epics and accounts on island life, as evidenced by Homer’s Odyssey, Sheherazade’ tales on Sindbad, and the Atlantis myths. The romantic novel was nourished in the same medium, as evidenced by Gulliver, Robinson Crusoe, and The Treasure Island.

In island literature exaggerations are almost mandatory. The scientific literature on islands, of course, does not allow exaggerations but there is still a marked tendency to focus on island organisms or phenomena that are peculiar in one way or another. No island birds are more commonly known as the monstrous Mauritius dodo and hardly any island plants as admired as the Seychelles giant coco or the silver sword of Hawaii. This trend to concentrate on the odd island organisms (the dodo approach, Adsersen 1995) is of course fascinating but it does not tell the whole truth on island biology. Neither does the focus on peculiar insular processes like evolutionary radiation as shown by Darwin finches or Hawaiian honeycreepers. No matter how seminal this approach (the finch approach) has proven to be for ecology and evolutionary biology it elucidates only part of the island scenario. The good stories on dodos and finches have the mark of anecdotes as long as they are not compared to something else. This “something” could be the rest of the organisms in the island, or the organisms of comparable areas on continents, or a general global pattern. In other words, it is necessary to consider the island biota as entities that may be quantitatively assessed and characterized.

MacArthur and Wilson’s classical works constitute a paradigmatic breakthrough of this approach, and by their work island biogeography was established as a discipline (MacArthur and Wilson 1967). Their equilibrium theory of island biogeography (ETIB) has been cyclically admired, criticized, rejected, reformulated, and modified ever since their modest-looking book was published, and this discourse will probably go on. But everyone participating in this debate acknowledges that island biotas may and should be assessed quantitatively and that island biotas are dynamical entities subject to qualitative and quantitative changes in time and space. Maybe this is the kernel of their message, and maybe its simplicity is the reason why it has had such a profound impact on evolutionary science, biogeography, and (macro)ecology. Now when the first forty years of island biogeography has been celebrated by a magnificent symposium at Harvard it seems apposite to ask whether Mac Arthur and Wilson had any predecessors in this quantitative approach. Marc Lomolino in his contribution to the symposium did so, focusing mainly on the American arena. Here I wish to draw attention to some important European contributors to early island biogeography.

Right after the publication of The Theory of Island Biogeography there was a marked tendency to try to support or even prove the theory by demonstrating mathematical relationships between species richness S and area A (species-area relationships, SPAR). Nice SPARs like the Arrhenius equation (log S = C + z logA) or the Gleason equation (S = K + p logA) (Gleason 1922) may be found by the quantitative approach and they may be result of ETIB; but ETIB could be explained by several other mechanisms, so there is no direct link between SPAR and ETIB. SPARs are important (“Ecology’s most general pattern”, Lomolino 2000) but not limited to island biogeography. Even Arrhenius’ pioneering work (Arrhenius 1921) was not an island biogeography work: it was indeed done on islands in the Stockholm archipelago but his S and A assessment were done in nested plots within the islands, so he could only obtain monotonously increasing functions, and there is no reference to total island S or A. Maybe Darlington’s rule of thumb (tenfold island area yields double species number, or S = c Alog 2 = c A0.301) is the first SPAR employed on true island entities (Darlington 1957). Numerous reviews and textbooks enlighten the history and relations between SPAR and ETIB.

SPARs are based on numbers of species S in limited, defined areas. Islands normally have hard borders and well-defined area, so that S may be assessed rather precisely.
It is therefore not surprising that some of the first quantitative data in biogeography are number of species on islands. J.D.Hooker studied Darwin’s plant collections from Galápagos and published in 1847 a remarkable treaty: On the Vegetation of the Galapagos Archipelago, as compared with that of other Tropical Islands and of the Continent of America. He set up three main questions to answer:

• How are the species distributed into major taxonomical groups?
• How many species are “peculiar” (endemic) and where do the species with wider distributions occur elsewhere?
• How are the species distributed within the archipelago?

Hooker not only tried to answer the questions but also managed to compare the patterns to that of other tropical archipelagos and to continental situations. His approach to question 3 is especially interesting. It is a numerical analysis of the number of plant species (the Florulæ) of the 4 islands that Darwin visited. In this analysis he repeatedly related the number of “peculiar” species to the total flora, and he even presented the data in a clear tabular form.

Table I. Original Hooker’s data on the florulæ of the Galápagos Islands.

His material was not complete, of course, even if he apparently managed to get access to all herbarium material in England and France. His estimate of total species number was 265, of which 17 were considered introduced by man. Today we assume that S ~ 600 and the number of naturalized plant species about the same. In the table beneath the modern figures (based on Lawesson et al 1987) are inserted. None of Hooker’s conclusions will hold but considering that only four of the major islands were included some of the relative figures (e.g. percent of plants confined to Galápagos) are quite accurate.

Table II. Hooker’s data on the florulæ of the Galápagos Islands. Recent data inserted. In the column “Absolutely peculiar to the islet.” the inserted column to the right left refer to the four islands mentioned, the one to the left refer to the entire archipelago.

Hooker’s approach is quite modern and for his time extraordinarily quantitative, although we today to each question would add “and why?” He maintained his interest in islands throughout his career, maybe best expressed in his lecture to the British Association in 1866 (reprinted and commented in Williamson 1984). In this lecture, which admittedly is much more verbal than numerical, he builds up both anecdotal and quantitative evidence that the pattern we may observe in island biogeography can be explained only if we assume evolution (“derivative origin of species”), and that the derivate origin of species became evident ”when Zoology and Botany became the subjects of exact scientific studies”! So certainly Hooker should be regarded as one of the progenitors of quantitative island biogeography.

Half a century after Hooker’s lecture a Finnish botanist, Alvar Palmgreen, meticulously censused the flora of islands in the Åland Archipelago of the Gulf of Bothnia, and remarkable papers followed: “The species richness as a plant geographical parameter” – “Chance as a plant geographical parameter” – “Remoteness as a plant geographical parameter”. The papers were in German and Swedish – they were read at the time but also forgotten. Haila and Järvinen, however, call to the attention that Palmgreen not only studied species-area relationships; species isolation relationships, and stochasticity in species dispersion but also came very close to formulation of ETIB (Haila and Järvinen 1982). It is, however, difficult to read Palmgren’s papers, even if you understand the language. His style is very wordy and even if he compares quantities like species number or isolation he does it verbally. There is hardly one graph or one mathematical formulation in his entire opus. Nevertheless, as Haila and Järvinen expressed it, his thoughts antedate MacArthur’s and Wilson’s by half a century.

Christen Raunkiaer in 1902

Christen Raunkiær from Denmark was contemporary with Palmgreen, but unlike Palmgreen he was not forgotten. His life forms, frequency analyses, and contemplations on species abundance distributions are still cited in most modern text books on ecology and biogeography. His life form system was outlined in Danish in 1904 (Raunkiær 1904). Next step was to introduce the system and its application in biogeography, which he did in French in a preliminary form in 1906. The final version came in 1907 in his most renowned publication Planterigets Livsformer og deres Betydning for Geografien. (The Life-Forms of plants and their bearing on geography) (Raunkiær 1907). The system was immediately seized by Scandinavian and continental botanists and ecologists. It became almost as paradigmatic in ecology as ETIB and it is quite apposite to celebrate its first century together with ETIBs 40 years. His works were after a long delay translated to English with the title: “The Plant Life Forms and Statistical Plant Geography” (Raunkiær 1934) and world wide acknowledged.

There are probably two reasons why Raunkiær’s life form system attained its high regard: The one is that the life forms are based on clear logical and biological reasoning and any plant species can without to much difficulty be categorized even by non-experts – and the second is his strict quantitative approach. With his own words: “-then Plant Geography as a botanical science gives place to Plant Geography as a geographical science” His combination of clear-cut concepts and exact biogeographical analyses on large scales made it possible for him to formulate precise definitions of biomes and to compare plant communities across biomes.The same combination is one of the reasons for MacArthur and Wilson’s success.

Even though the word “statistical” recurs in several of Raunkiær’s titles, he had no great knowledge on statistics as practiced today. Parametric distributions, hypothesis testing and significance were concepts unknown to him, as they where to Hooker, Palmgreen and Arrhenius. First after Fischer’s paradigmatic contributions to statistics these concepts became applicable to biogeographers and soon important contributions emerged. Within island biogeography Preston’s monumental papers on Commonness and Rarity of Species (Preston 1948, Preston 1962) seem to be best known but the equally monumental monograph Patterns in the Balance of Nature by C.B. Williams (1964) (a coworker of Fischer’s) deserve as much recognition. Both Preston and Williams took their approach from abundance distributions (lognormal and logseries, respectively) in communities and ended up by reflecting on SPARs – very much fertilizing the ground for ETIB.

Figure 1. The Raunkiaerian J

Abundance distribution was another of Raunkiær´s interests. He invented the frequency analysis in vegetation ecology and observed the recurring pattern known as the Raunkiærian J (Figure 1). He even postulated that mature homogeneous vegetation could be recognized by this pattern. Such a daring postulate would of course raise discussion. McIntosh (1962) reviewed the discussion and concluded that the Raunkiærian J is one of those “ideas that seems to be invulnerable to attack and persist although subjected to multiple executions” (another parallel to ETIB?). Raunkiær’s observation was a seminal inspiration for Preston (1948) and he demonstrated that the Raunkiaerian J may be derived from the lognormal abundance distribution, (which on its side will lead to the Arrhenius equation). Later on Williams (1964) showed that it may be derived also from the logseries distribution (which lead to Gleason equation). Even very recently the Raunkiærian J attains attention, now under the more general term “hollow species abundance distributions” (McGill et al 2007).

It is less known that one of Raunkiær’s last publications was on island biogeography: The Life-Form Spectrum of Some Atlantic Islands. The reason why it is almost forgotten is that it appeared in the series Botaniske Studier (published by himself) that comprises several of his emeritus works. It is an 80 page monograph in which he compares the life-form spectra of most Atlantic archipelagos from Svalbard in the north to South Georgia in the south. His questions were almost the same as Hooker’s first two questions above, except that, instead of taxonomical supraspecific groups, he considered ecological ones:

1. How are the species distributed into life-form groups?
2. How many species are “peculiar” (endemic) and does their life-form spectrums differ from that of species with wider distributions occur elsewhere?

He also added a “why” to his question – and found that his climatically derived life form biome types give good explanations. His discussion on this is lengthy because he had not the necessary tools to make up the relevant exact evaluations but he would probably have been pleased to see the ordination diagram in figure 2. It is based on his data, and however incomplete they may have been they give very good support to his ideas.

Figure 2. Nonmetric multidimensional scaling of Raunkiær’s data on life form spectra from Atlantic islands. The ordination was run in PC-ORD 5 with Euclidian Distance as dissimilarity measure. The diagram is highly significant (P<0.01,>

Raunkiær was not the first to use quantitative data in biogeographical analyses. Early biogeographers like Schouw, De Candolle, Hooker and Warming used quantitative expressions to support their idea. The novelty in his approach was that he demanded and devised exact methods to gather the data and from the emerging patterns he generated his general ideas.Thus, even if his missed the mathematical and statistical skill of today he must be regarded as a pioneer of exact quantitative analyses of biogeographical data. He was very keen on this approach. Already in his first paper on frequency analysis (Raunkiær 1909) he expresses his motto: Numbers are the poetic meters of science (Tal er videnskabens versefødder). In this light it is not surprising that he chose 1000 plant species selected at random from the Index Kewensis when he set up his “normal” life form spectrum, and that he based his species abundance distribution J on 1000 vegetation analysis from all over the world.

Christen Raunkiaer around 1935

According to the many anecdotes told about him at the University of Copenhagen his exactitude gave the impression that he was pedantic and, as he also was rather introverted, he was not liked by his students – they rather feared him. In his time as professor ordinarius of botany (1911-1923) he had residence in the Botanical Garden and he insisted that the students use the garden as a living book of botany. Part of his teaching was questioning the students whenever he met them and often rather brusquely so. But at one point he surprised all the students because instead of all his unpleasant questions he just asked them to fold their hands – he then observed them, nodded, thanked and left them puzzled. The numbers he gathered was how many of them had the right thumb on top. Many of us know this analysis to be a classic in elementary statistical textbooks. Raunkiær may very well have been the first to make an exact count (on 1000 persons??). So he was actually very broadminded in his pedantry. Anyway, he took up his demanding behavior towards the students again, so much that the students sent a timid delegate to the professor to ask politely for a change. His response was remarkable: he looked coldly at the shivering student and said: ”I will not change my methods or my demands, but if the students are not satisfied by my teaching I will resign!” - and so he did, at an age of 63. This secured him a rather long emeritus period where he had peace to pursue his whims.

The allusion to poetry in his motto is another sign of his wider view. He must have been a keen reader of poetry. After his retirement he started “botanizing” in Danish poetry and he applied his “frequency analysis” as a method to characterize poets and epochs. The sample units were not circular area samples but verse lines and the observed objects were plant names. He ploughed through millions of verse lines written by hundreds of poets – so there was a need to define what a true poet is: It is a person who has published at least 1000 verse lines or one volume of poems. He determined the plant species spectrum for each of these poets in terms of total species richness and abundance distribution (abundance measured by number of mentions/1000 verse lines). So if you are interested and dedicated (and able to read Danish) you may learn that the neoclassicistic period had a much lower species richness and density then the romantic period, that Hans Christian Andersen was only the second Danish poet to mention heather, and that it is possible to distinguish between poets from Jutland and Zeeland by their predominant species. The style and stringency in his three publications on such matters are brilliant – and fun to read.

Shortly before he died he took up his old interest in plant geography. In one paper he adresses the relationship between range, species-genus ratio, and life forms. He selected the 10 largest plant families with in total 2772 genera and 43594 species (his own count!). He was able to show that genera that comprise more than one life form have considerable higher species to genus rate, and a wider geographical range. This search on the global scale for relationships between geographical features, taxonomical features and functional traits/types is a focal approach in biogeography even now.

And now we return to his island biogeography paper. It is from the same period, and apart from its undisputed scientific relevance it also contains statements about attitudes and sentiments that are shared by island biogeographers today. For instance its first sentence: “Islands, especially isolated oceanic islands, have always held a fascination for me, both emotionally and intellectually” – which happens to be the first sentence also of this essay. Thus, even if Raunkiær never would have ventured to add exaggerations or fantasies to his scientific publications, he certainly did not refrain from showing his sentiments. He also expresses modesty and self critique. His motto: ”Numbers are the poetic meters of science” is the prologue paragraph of his “Investigations and statistics of plant formations” from 1909. The paper has also an epilogue: ”Numbers are the poetic meters of science. Verses may halt, and so also may the numbers of science. I hope the numbers given in this work will be found to halt no more than their human origin inevitably entails”. This paragraph has never been more apposite than now: Biogeographers must remember that their brilliant theories and sophisticated models build on numbers (field data) that are of human origin, and as such they will sometimes halt so much that the entire theoretical construction becomes highly tottering.

Additional information about Christen Raunkiær including a complete list of his works and some biografies can be found at http://www.macroecology.ku.dk/resources/default.asp?p=Raunkiaer

References
Adsersen, H., 1995: Research on Islands: Classic, Recent, and Prospec­tive Approaches. In: Vitousek, P.M., Loope, L.L. and Adsersen, H. (Eds.): Islands: Biological Diversity and Ecosystem Func­tion. Ecologi­cal Studies vol 115, Springer, Heidelberg, pp.8-21.
Arrhenius, O. 1921. Species and area. - J. Ecol. 9: 95-99.
Darlington, P.J. 1957. Zoogeography. Wiley
Gleason, H. A. 1922. On the relation between species and area. - Ecology 3: 158-162.
Haila, Y. and Järvinen , O. 1982 The role of theoretical concepts in understanding the ecological theatre: a case study in island biogeography. – In Saarinen, E. (Ed.): Conceptual Issues in Ecology: 261-278. D. Riedel Publishing Company.
Hooker, J. D. 1847. On the vegetation of the Galapagos Archipelago, as compared with that of some other tropical islands and of the continent of America.- Transactions from the Linnean Society of London 20: 235-262
Lawesson, J. E., Adsersen, H. and Bentley, P. 1987. An updated and annotated check list of the vascular plants of the Galápagos Islands. - Reports from the Botanical Institute, University of Aarhus, 16.
Lomolino. M.V., 2000. Ecology’s most general, yet protean pattern: The species-area relationship.- Journal of Biogeography. 27: 17-26.
MacArthur, R. H. and Wilson, E. O. 1967. The Theory of Island Biogeography. - Princeton University Press. Princeton
McGill B. J. et al (17 coauthors) 2007: Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecology Letters 10: 995-1015
McIntosch,R.P. 1962. Raunkiaer’s “law of frequency”. Ecology 43: 533-535
Palmgreen, A. 1922: Über Artenzahl und Areal sowie über die Konstitution der Vegetation. Eine vegetationsstatistische Untersuchung. Acta Forestalia Fennica 22:1-136.
Palmgreen, A. 1921. Die Entfernung als Pflanzengeographischer Faktor. – Acta Societas pro Fauna et Flora Fennica 49: 1-113
Palmgreen, A 1925. Die Artenzahl als Pflanzengeographischer Charakter sowie Der Zufall und die Sekuläre Landhebung als Pflanzengeographischer Faktoren. - Fennia 46: 1-139
Preston, F.W. 1948: The commonness, and rarity, of species. Ecology 29: 254-283
Preston, F.W. 1962.The canonical distribution of commonness and rarity: Part I: Ecology 43: 185-215, Part 2: Ecology 43: 410-432
Raunkiær, C. 1904. Om biologiske Typer, med Hensyn til Planternes Tilpasning til at overleve ugunstige Aarstider. Botanisk Tidsskrift 26: 14
Raunkiær, C. 1905. Types biologiques pour la géographie botanique. Videnskabernes Selskabs Oversigter 1905: 347-438
Raunkiær, C. 1907. Planterigets Livsformer og deres Betydning for Geografien. Copenhagen.
Raunkiær, C. 1909. Formationsundersøgels og Formationsstatistik. Botanisk Tidsskrift 30: 20-132
Raunkiær, C. 1930: Hjemstavnsfloraen hos Hedens Sangere Blicher og Aakjær. Schultz forlag, København.
Raunkiær, C. 1934. The Life Forms of Plants and Statistical Plants Geography being the collected Papers of C. Raunkiaer. Clarendon press, Oxford.
Raunkiær, C. 1936. The Life-form Spectrum of some Atlantic Islands. Botaniske Studier 4: 240-328
Raunkiær, C. 1937. Life-form, genus area, and number of species. Botaniske Studier 5: 343-356
Williams, C.B. 1964: Patterns in the Balance of Nature. Academic Press, London
Williamson 1984. Sir Joseph Hooker’s Lecture on Island Floras. – Biological Journal of the Linnean Society 22: 55-77

‘Pleistocene re-wilding’ merits serious consideration also outside North America

Jens-C. Svenning, Department of Biological Sciences, University of Aarhus, Ny Munkegade, Build. 1540, DK-8000 Aarhus C, Denmark.

Recently, Josh Donlan and coworkers have argued for ‘Pleistocene re-wilding’ as a new optimistic agenda for 21^st century conservation in North America (Donlan et al., 2005, 2006; Donlan, 2007). Pleistocene re-wilding refers to the re-establishment of a megafauna similar to that which disappeared from that continent roughly 13,-11,000 years ago. Re-wilding would be achieved by establishing closely related and functionally similar extant extra-regional species as replacements for their extinct counterparts. Donlan and coworkers provide a number of justifications for their proposal, including the ecological services such as grassland maintenance provided by large vertebrates, the re-establishment of the evolutionary potential of the megafauna, and the provision of safe havens for extant megafauna species. The re-wilding proposal has generated a much controversy. One potential problem that has been pointed out repeatedly is that reintroducing proxies of species that have been extinct for 10,000 years or more may damage current biodiversity, just like invasive species are known to do, as ecosystems have changed and evolved after the Pleistocene extinctions (e.g., Rubenstein et al., 2006).

The purpose of the present paper is not to repeat this debate, but to point out that Pleistocene re-wilding deserves serious consideration also outside North America. During the last 50,000 years megafaunas have been decimated not only in North America, but on an essentially worldwide basis. Although an issue of perpetual controversy, there is increasing evidence that modern humans were the ultimate cause of this global event (e.g., Barnosky et al., 2004). Pleistocene re-wilding is already being implemented in a large-scale Siberian project with the stated aim of preserving and extending Pleistocene-like grasslands at northern latitudes, http://news.bbc.co.uk/1/hi/sci/tech/4533485.stm. However, Pleistocene re-wilding could be much more broadly considered.

Upper Pleistocene (warm period) landscape from Northern Iberian Peninsula, with European bisons, deer and ibexes (illustration by Mauricio Antón; http://www.mauricioanton.com/).

Here, I would like to highlight Europe as an obvious place to begin re-wilding projects (see also the article at http://www.sciam.com/). While continental Europe lost many megafauna species during the latest Pleistocene and Holocene, most still survive elsewhere, have close relatives that do, or survive in domesticated form (the main exceptions are the scimitar cat (Homotherium latidens), cave bear (Ursus spelaeus), woolly mammoth (Mammuthus primigenius), woolly rhinoceros (Coelodonta antiquitatis), steppe rhinoceros (Dicerorhinus hemitoechus), and giant deer (Megaloceros giganteus); Kurtén, 1968; Stuart, 1991). In this aspect Europe differs strongly from the Americas; where a much larger proportion of the extinct megafauna have no close extant counterparts, e.g., ground sloths, glyptodonts, sabertoothed cats, short-faced bear, giant beaver etc. In further contrast to the Americas, many megafauna species did not disappear from Europe until well into the Holocene. Therefore, the invasive species analogy is hardly applicable in Europe and in general negative ecological or biodiversity impacts on a broad scale are hard to imagine. Hence, megafauna re-establishment would seem particularly feasible and logical in this region.

A European re-wilding strategy should obviously include the megafauna species still extant in Europe, many of which have strongly reduced ranges today, e.g. wolf (Canis lupus), brown bear (Ursus arctos), lynx (Lynx lynx), wild boar (Sus scrofa), moose (Alces alces), and European bison (Bison bonasus). In fact, many of these species have already been re-introduced to parts of their former ranges, the most noteworthy case being the European bison, which went completely extinct in the wild during the early 20^th century, but today is re-established in scattered localities throughout Eastern Europe (Mitchell-Jones et al., 1999) and seriously considered for re-establishment in Germany (e.g., the subject of a 2007 workshop “European bison in Central European landscapes – experiences and perspectives”, organized by the German Federal Agency for Nature Conservation).

Two large mammal species have already been re-established in Europe following their earlier complete extinction on this continent:

• The fallow deer (Dama dama) was widespread in Europe under temperate conditions during the Late Pleistocene and survived into the Holocene in the Balkans (Kurtén, 1968; Bökönyi, 1971). While it is doubtful whether any autochthonous European populations made it to the present day, the species survived in Asia Minor and is now widespread in Europe thanks to several millennia of re-introductions (Mitchell-Jones et al., 1999).

Fallow deer (Dama dama) is now again widespread in Europe, following several millenia of re-introductions (photo: Biopix.dk [J.C. Schou]; http://www.biopix.dk/).

• The musk ox (Ovibos moschatus) occurred in Europe under cold climatic conditions until the late-glacial (Stuart, 1991), but small populations have now been re-established in the Scandinavian mountains since the middle of the 20^th century.

In neither case has the re-introductions caused these species to widely displace extant native species.

Group of species from the Lezetxiqui deposit (Upper Pleistocene; Guipúzcoa, Basque Country). This drawing shows the species currently extinct in the Iberian Peninsula. Other species still present in the Peninsula have been also found at this deposit, such as wolves, foxes, deers, chamois, wild boars, etc. (illustration by Mauricio Antón; http://www.mauricioanton.com/).

In addition to the above species a number of other large mammal species that became extinct in Europe during the latest Pleistocene or Holocene could also be considered in a European re-wilding strategy:

In a number of cases the species in question still survives outside Europe, although often under precarious circumstances:

• Lion (Panthera leo): An obvious candidate for re-establishment would be the Asiatic lion (ssp. persica), now restricted to just 300+ individuals in a very limited region in India (http://en.wikipedia.org/wiki/Asiatic_lion): Lions probably belonging to this subspecies occurred in the Balkans as far north as Hungary just a few thousand years ago, while lions also persisted into the early Holocene in the northern Iberian Peninsula (Vörös, 1983; Sommer and Benecke, 2006). Furthermore, lions of the extinct spelaea subspecies were widespread in Europe until the end of the last glacial, perhaps mixed with the modern Asiatic subspecies in Eastern Europe (Stuart, 1991; Yamaguchi et al., 2004).
• Leopard (Panthera pardus), spotted hyena (Crocuta crocuta), and dhole or Asiatic wild dog (Cuon alpinus): These large predators were widespread in Europe during the Late Pleistocene, with the leopard possibly still occurring in Greece into historic times, and the spotted hyena and dhole having last occurrences during the late-glacial (Kurtén, 1968; Stuart, 1991; Stewart, 2004; Sommer and Benecke, 2005, 2006; Voultsiadou and Tatolas, 2005). Of these, the leopard is declining, with several of its subspecies in danger of extinction or already extinct, while the dhole has just 2,500 free-living individuals and is declining as well (http://www.iucnredlist.org/).
• Horse (Equus caballus) and cattle (Bos taurus): Both species were widespread in Late Pleistocene and Holocene Europe, but went extinct in wild form within the last 400 years. However, both species still exist in domesticated and feral form in Europe and de-domesticated forms are already being used in local re-wilding projects, see e.g. http://en.wikipedia.org/wiki/Oostvaardersplassen.

The konik is a small semi-wild horse race that is similar to and partially descended from the last originally wild horses of Europe. It is increasingly used in the management of natural areas; here, Lille Vildmose in Denmark (photo: Biopix.dk [J.C. Schou]; http://www.biopix.dk/).

Aurochs-like de-domesticated cattle is increasingly used in the management of natural areas in Europe; here, Lille Vildmose in Denmark (photo: Biopix.dk [J.C. Schou]; http://www.biopix.dk/).

• Asiatic wild ass (Equus hemionus): This species occurred in south-eastern Europe into the Medieval Period (Willms, 1989). Furthermore, it could be introduced in Europe’s drier regions a proxy for the closely related (conspecific?), extinct European wild ass (Equus hydruntinus), which was widespread in Europe during the Late Pleistocene and far into the Holocene, probably surviving in Portugal and Spain into medieval times and possibly as late as 1540 AD (Kurtén, 1968; Uerpmann, 1976; Vörös, 1981; Willms, 1989; Nores Quesada and Von Lettow-Vorbeck, 1992; Burke et al., 2003; Antunes, 2006; Orlando et al., 2006). The noun zebro was originally for this species, but was later transferred to the African striped equid by Iberian explorers (Nores Quesada and Von Lettow-Vorbeck, 1992; Antunes, 2006). The Asiatic wild ass is listed as vulnerable by the IUCN and has several critically endangered or extinct subspecies (http://www.iucnredlist.org/).
• The hippopotamus (Hippopotamus amphibius): The modern species was common in the Late Pleistocene Europe under warm-temperate conditions (e.g., in the Thames river during the last interglacial), probably becoming extinct on the European continent relatively early during the last glacial (Kurtén, 1968; Stuart, 1991; van Kolfschoten, 2000). Currently, the hippopotamus is declining in its African range and is listed as vulnerable by the IUCN (http://www.iucnredlist.org/).

Some large mammal species that went extinct not only in Europe, but also globally during the Late Pleistocene have extant relatives that could be re-introduced as ecological and evolutionary proxies:

• Asiatic elephant (Elephas maximus): This species could be used as a proxy of the closely related straight-tusked elephant (Elephas [Palaeoloxodon] antiquus), which was widespread in Europe under warm- to cool-temperate conditions during the Late Pleistocene (Kurtén, 1968; Poulakakis et al., 2002). The straight-tusked elephant became extinct in continental Europe during the middle part of the last glacial (Mol et al., 2007), but Mediterranean island dwarf forms survived later, notably until <4,000 st="on">island of Tilos (Stuart, 1991). It is worth noting that the Asiatic elephant is not an exclusively tropical species, but was widespread in temperate China during earlier in the Holocene (e.g., Tong and Patou-Mathis, 2003; http://www.nature.com/nature/journal/v430/n6999/full/430505a_fs.html). Currently, wild populations are declining and the species is listed as endangered (http://www.iucnredlist.org/).

Upper Pleistocene landscape from Madrid (Central Iberia), with wolves, deers, wild horses, aurochs (wild cattle, Bos primigenius) and mammoths (illustration by Mauricio Antón; http://www.mauricioanton.com/).

• The water buffalo (Bubalus bubalis): This Asian species could be used as a proxy for the extinct species B. murrensis, which occurred under warm-temperate conditions in Europe at least until the last interglacial (Kurtén, 1968; van Kolfschoten, 2000). The wild water buffalo is endangered and now its numbers are below 4,000 individuals (see http://www.iucnredlist.org/).
• Sumatran or hairy rhinoceros (Dicerorhinus sumatrensis): If saved from the brink of extinction (e.g., http://en.wikipedia.org/wiki/Sumatran_Rhinoceros), this species of mountainous forest regions in Southeast Asia could possibly be used as a proxy for the extinct Merck’s rhinoceros (D. kirchbergensis), a temperate forest species that became extinct during the last glacial (Kurtén, 1968).

In recent years the ecological role of large herbivores in European nature has been much debated (e.g., Vera, 2000; Svenning, 2002), and more or less free-ranging large herbivores are increasingly re-introduced to aid the management of natural areas. Moreover, as already mentioned Europe has already made successful experiences with megafauna re-introductions, notably European bison, fallow deer, and musk ox. Clearly, given the particularly good possibilities for re-establishing a near-complete European megafauna and the precarious circumstances under which many of the candidate species exist outside Europe, Pleistocene re-wilding deserves to become more broadly considered in European nature conservation.

Upper Pleistocene (cold period) landscape from Northern Iberian Peninsula, with mammoths, woolly rhinoceros, lions, reindeers and wild horses (illustration by Mauricio Antón; http://www.mauricioanton.com/).

This is not to say that there will not be many, difficult cultural and sociological challenges to the implementation of full-scale Pleistocene re-wilding in Europe, perhaps even more so than in North America. Many of the candidate species require large areas and some, such as lions, are dangerous to humans. It may seem unrealistic to find living space for such animals in densely populated Europe. However, it is important to remember that the areas in Asia and Africa where the candidate species occur today also are home to large and growing numbers of people. To achieve long-term preservation of Earth’s magnificent megafauna as evolutionary and ecologically viable, free-living species will require solutions that allow humans and large, dangerous animals to coexist.

References

Antunes, M. T. (2006) The Zebro (Equidae) and its extinction in Portugal, with an appendix on the noun zebro and the modern "zebra". Equids in time and space (ed. by M. Maskour), pp. 210-235. Oxbow Books, Oxford.

Barnosky, A. D., Koch, P. L., Feranec, R. S., Wing, S. L., & Shabel, A. B. (2004) Assessing the causes of late Pleistocene extinctions on the continents. Science, 306, 70-75.

Bökönyi, S. (1971) Angaben zum frühholozänen Vorkommen des Damhirsches, Cervus (Dama) dama (Linné, 1758), in Europa. Säugetierkundliche Mitteilungen, 19, 206-217.

Burke, A., Eisenmann, V., & Ambler, G. K. (2003) The systematic position of Equus hydruntinus, an extinct species of Pleistocene equid. Quaternary Research, 59, 459-469.

Donlan, C. J. (2007) Restoring America's big, wild animals. Scientific American, June, 70-77.

Donlan, C. J., Berger, J., Bock, C. E., Bock, J. H., Burney, D. A., Estes, J. A., Foreman, D., Martin, P. S., Roemer, G. W., Smith, F. A., Soulé, M. E., & Greene, H. W. (2006) Pleistocene rewilding: an optimistic agenda for twenty-first century conservation. American Naturalist, 168, 660-681.

Donlan, J., Green, H. W., Berger, J., Bock, C. E., Bock, J. H., Burney, D. A., Estes, J. A., Foreman, D., Martin, P. S., Roemer, G. W., Smith, F. A., & Soulé, M. E. (2005) Re-wilding North America. Nature, 436, 913-914.

Kurtén, B. (1968) Pleistocene mammals of Europe. Weidenfeld and Nicolson, London.

Mitchell-Jones, A. J., Amori, G., Bogdanowicz, W., Kryštufek, B., Reijnders, P. J. H., Spitzenberger, F., Stubbe, M., Thissen, J. B. M., Vohralík, V., & Zima, J. (1999) The atlas of European mammals. T & AD Poyser Ltd. & Academic Press, London, UK.

Mol, D., de Vos, J., & van der Plicht, J. (2007) The presence and extinction of Elephas antiquus Falconer and Cautley, 1847, in Europe. Quaternary International, 169-170, 149-153.

Nores Quesada, C. & Von Lettow-Vorbeck, C. L. (1992) La zoologia historica como complemento de la arqueozoologia. El case del zebro. Archaeofauna, 1, 61-71.

Orlando, L., Mashkour, M., Burke, A., Douady, C. J., Eisenmann, V., & Hänni, C. (2006) Geographic distribution of an extinct equid (Equus hydruntinus: Mammalia, Equidae) revealed by morphological and genetical analyses of fossils. Molecular Ecology, 15, 2083-2093.

Poulakakis, N., Theodorou, G. E., Zouros, E., & Mylonas, M. (2002) Molecular phylogeny of the extinct Pleistocene dwarf elephant Palaeoloxodon antiquus falconeri from Tilos Island, Dodekanisa, Greece. Journal of Molecular Evolution, 55, 364-374.

Rubenstein, D. R., Rubenstein, D. I., Sherman, P. W., & Gavin, T. A. (2006) Pleistocene Park: Does re-wilding North America represent sound conservation for the 21st century? Biological Conservation, 132, 232-238.

Sommer, R. & Benecke, N. (2005) Late-Pleistocene and early Holocene history of the canid fauna of Europe (Canidae). Mammalian Biology, 70, 224-241.

Sommer, R. S. & Benecke, N. (2006) Late Pleistocene and Holocene development of the felid fauna (Felidae) of Europe: a review. Journal of Zoology, 269, 7-19.

Stewart, J. R. (2004) Neanderthal-modern human competition? A comparison between the mammals associated with Middle and Upper Palaeolithic industries in Europe during OIS 3. International Journal of Osteoarchaeology, 14, 178-189.

Stuart, A. J. (1991) Mammalian extinctions in the Late Pleistocene of northern Eurasia and North America. Biological Review, 66, 453-562.

Svenning, J.-C. (2002) A review of natural vegetation openness in north-western Europe. Biological Conservation, 104, 133-148.

Tong, H. & Patou-Mathis, M. (2003) Mammoths and other proboscideans in China during the Late Pleistocene. Deinsea, 9, 421-428.

Uerpmann, H.-P. (1976) Equus (Equus) caballus und Equus (Asinus) hydruntinus im Postpleistozän der Iberischen Halbinsel (Perissodactyla, Mammalia). Säugetierkundliche Mitteilungen, 24, 206-218.

van Kolfschoten, T. (2000) The Eemian mammal fauna of central Europe. Netherlands Journal of Geosciences, 79, 269-281.

Vera, F. W. M. (2000) Grazing ecology and forest history. CABI Publishing, Oxon, UK.

Vörös, I. (1981) Wild equids from the early Holocene in the Carpathian Basin. Folia Archaeologica, 32, 37-68.

Vörös, I. (1983) Lion remains from the Late Neolithic and Copper Age of the Carpathian Basin. Folia Archaeologica, 34, 33-50.

Voultsiadou, E. & Tatolas, A. (2005) The fauna of Greece and adjacent areas in the Age of Homer: evidence from the first written documents of Greek literature. Journal of Biogeography, 32, 1875-1882.

Willms, C. (1989) Zum Aussterben des europäischen Wildesels. Germania, 67, 143-148.

Yamaguchi, N., Cooper, A., Werdelin, L., & Macdonald, D. W. (2004) Evolution of the mane and group-living in the lion (Panthera leo): a review. Journal of Zoology, 263, 329-342.

The drawings of the Iberian megafauna communities from the Upper Pleistocene that illustrate this article and the cover of this issue have been kindly handed over by Mauricio Antón. Mauricio is a Paleontological Artist, specialized in creating images that bring prehistoric creatures and their environments back to life. He has created artwork for museum exhibits worldwide, co-authored and illustrated numerous books and magazine articles, and collaborated with the BBC and Discovery Channel in developing several documentary films. He is also a regular collaborator of many Paleontologists. The results of his research on the anatomy of fossil vertebrates have been published several academic journals (e.g., Journal of Vertebrate Paleontology, Journal of Human Evolution or Proceedings of the National Academy of Sciences USA). Mauricio is currently exploring the applications of computer graphic imaging and animation to paleoart. Some of his books are:

Agustí, J. & Antón, M. (2002) Mammoths, Sabertooths, and Hominids. Columbia Universitiy Press, New York. (on the evolution of European mammal faunas)

Turner A. & Antón, M. (2004) Evolving Eden. Columbia University Press, New York. (on the evolution of African mammal faunas)

Antón, M. (2007) El secreto de los fósiles: El arte y la ciencia de reconstruir a nuestros antepasados (y otras criaturas). Aguilar, Madrid. [The secret of fossils: the art and science of reconstructing our ancestors (and other creatures)] (on the methods used to recreate past fauna from the deposit to the final result; not yet translated)

For further information see:
http://www.mauricioanton.com/
http://www.comunidadsmart.es/articulos_detalle.php?id=268 (in Spanish)