Getting the Measure of Biodiversity

insight review articles Getting the measure of biodiversity

Andy Purvis* & Andy Hector†

*Department of Biology and †NERC Centre for Population Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7PY, UK

The term ‘biodiversity’ is a simple contraction of ‘biological diversity’, and at first sight the concept is simple too: biodiversity is the sum total of all biotic variation from the level of genes to ecosystems. The challenge comes in measuring such a broad concept in ways that are useful. We show that, although biodiversity can never be fully captured by a single number, study of particular facets has led to rapid, exciting and sometimes alarming discoveries. Phylogenetic and temporal analyses are shedding light on the ecological and evolutionary processes that have shaped current biodiversity. There is no doubt that humans are now destroying this diversity at an alarming rate. A vital question now being tackled is how badly this loss affects ecosystem functioning. Although current research efforts are impressive, they are tiny in comparison to the amount of unknown diversity and the urgency and importance of the task.

o proceed very far with the study of biodiversity, and no single number can incorporate them both without we need to pin the concept down. We cannot loss of information. This should not be disappointing; even begin to look at how biodiversity is indeed we should probably be relieved that the variety distributed, or how fast it is disappearing, of life cannot be expressed along a single dimension. unless we can put units on it. However, any Rather, different facets of biodiversity can each be attemptT to measure biodiversity quickly runs into the quantified (Box 1). problem that it is a fundamentally multidimensional Knowing the diversity (however measured) of one place, concept: it cannot be reduced sensibly to a single group or time is in itself more-or-less useless. But, as we shall number1,2. A simple illustration can show this. Figure 1 discuss later, comparable measurements of diversity from shows samples from the insect fauna in each of two multiple places, groups or times can help us to answer habitats. Which sample is more diverse? At first sight it crucial questions about how the diversity arose and how we must be sample A, because it contains three species to might best act to maintain it. We shall see also how the sample B’s two. But sample B is more diverse in that there usefulness of the answers depends critically on the selection is less chance in sample B that two randomly chosen of an appropriate diversity measure. No single measure will individuals will be of the same species. Neither of these always be appropriate (indeed, for some conservation ques- measures of diversity is ‘wrong’ — species richness and tions, no single measure can probably ever be appropriate). evenness are two (among many) of biodiversity’s facets, The choice of a good measure is complicated by the frequent

Sample A Sample B

Figure 1 Two samples of insects from different locations, illustrating two of the many different measures of diversity: species richness and species evenness. Sample A could be described as being the more diverse as it contains three species to sample B’s two. But there is less chance in sample B than in sample A that two randomly chosen individuals will be of the same species.

Box 1 Parts of the whole: numbers, evenness and difference

Biodiversity has a multitude of facets that can be quantified. Here we Evenness classify some commonly used measures into three conceptually A site containing a thousand species might not seem particularly different (although not orthogonal) approaches. diverse if 99.9% of individuals that you find belong in the same species. Many diversity indices have been developed to convey the Numbers extent to which individuals are distributed evenly among species2. The most commonly considered facet of biodiversity is species Most but not all combine evenness with species richness, losing richness — the number of species in a site, habitat or clade. Species information by reducing two dimensions to one. There are genetic are an obvious choice of unit when trying to measure diversity. Most analogues of these indices100, such as heterozygosity, that people have an idea what ‘species’ means and, although their ideas incorporate both allele number and relative frequencies. differ considerably (reviewed in ref. 96), there is even less commonality about other levels in the taxonomic hierarchy30 (Fig. 3). Difference Many other measures are less intuitive, and have arisen only through Some pairs of species (or alleles or populations) are very alike, whereas appreciation of limitations of measures of species richness. Species others are very different. Disparity101 and character diversity93 are are also sensible units to choose from a biological perspective: they measures of phenotypic difference among the species in a sample, and keep their genes more or less to themselves, and to that extent have can be made independent of species number. Some phenotypic independent evolutionary trajectories and unique histories. The characteristics might be considered more important than others, for current ‘best guess’7 is that there are around 14 million species, but instance the ecological diversity among species may be crucial for this is very much a provisional working figure. Regions with many ecosystem functioning. Genetic variability among populations can also species, especially endemic species, are sometimes called be measured in various ways100. If populations within species differ hotspots97. enough either genetically or phenotypically, they may be considered to Species and regions differ in their number of populations. be subspecies, management units or evolutionarily significant units102; Populations of a given species, if defined on the basis of limited gene numbers of these therefore provide estimates of difference. All these flow among them, will evolve to an extent independently. Each kinds of difference are likely to be at least partly reflected by the population contributes additional diversity. The number of genetic phylogenetic diversity103 among organisms, which is estimated as the populations in the world has been estimated to lie between 1.1 and 6.6 sum total of the branch lengths in the phylogeny (evolutionary tree) linking billion66. them. Species or populations differ in the numbers of alleles they have at Sample in different places, and you will find different things. This given loci. For instance, Mauritius kestrels (Falco punctatus) have lost spatial turnover itself has many facets2 (for example, beta diversity, over half of the alleles present historically at 12 sampled microsatellite gamma diversity and numbers of habitat types), and important loci98. consequences for any attempt to conserve overall diversity (see Moving above the species level, higher-taxon richness is often review by Margules and Pressey, pages 243–253, and refs 104, 105). used in studies of biodiversity, usually as a less data-demanding Likewise, temporal turnover106 is the extent to which what is found surrogate for species richness99. changes over time. need to use surrogates for the aspect in which we are most interest- below the surface; these subsurface lithoautotrophic microbial ed3,4. Surrogacy is a pragmatic response to the frightening ignorance ecosystems (termed SLiMEs) may have persisted for millions of years about what is out there. Some recent discoveries highlight just how without any carbon from the surface10. Controversy surrounds much we probably still do not know. another proposed discovery: whether or not the 100-nm-diameter nanobacteria found in, among other places, kidney stones are living The growing biosphere organisms11. At an even smaller scale, genomes provide fossils Technological advances and the sense of urgency imparted by the rate that indicate great past retroviral diversity12. Genomes have also of habitat loss are combining to yield discoveries at an incredible rate. been found to provide habitats for many kinds of genetic entity — This may seem surprising, given that expedition accounts of natural transposable elements — that can move around and replicate historians from the 18th and 19th centuries conjure up images of dis- themselves. Such elements can provide important genetic variation covery on a grand scale that seemingly cannot be matched today — to their hosts, can make up more than half of the host’s genome13, and look in the rocks … a new fossil mammal; look in the lake … a new have life histories of their own14. fish genus; look on the dinner plate … a new species of bird. Finding There are two other ways in which the biosphere can perhaps be new large vertebrates nowadays is indeed newsworthy, but a new said to be growing. The first is that the rate at which taxonomists split species of large mammal is still discovered roughly every three years5 one previously recognized species into two or more exceeds the rate and a new large vertebrate from the open ocean every five years6. And at which they lump different species together, especially in taxa that most organisms are much smaller than these are. An average day sees are of particular concern to conservationists (for example, the formal description of around 300 new species across the whole platyrrhine primates15). Part of the reason is the growing popularity range of life, and there is no slowdown in sight. Based on rates of dis- of one way of delimiting species — the phylogenetic species concept covery and geographical scaling-up, it seems that the roughly 1.75 (PSC)16 — under which taxa are separate species if they can be diag- million described species of organism may be only around 10% of the nosed as distinct, whether on the basis of phenotype or genotype. If total7. the PSC becomes widely applied — which is a controversial issue17 — It is not only new species that are discovered. Cycliophora and then the numbers of ‘species’ in many groups are sure to increase Loricifera are animal phyla (the level just below kingdom in the taxo- greatly18 (although the amount of disparity will barely increase at all). nomic hierarchy) that are new to science in the past 20 years8. Within A second way in which the catalogue of diversity is growing is that the Archaea, the discovery of new phylum-level groups proceeds at computer databases and the Internet are making the process of infor- the rate of more than one a month9. The physical limits of the bios- mation gathering more truly cumulative than perhaps ever before. phere have been pushed back by the recent discovery of microbial Some existing sites serve to provide examples of the information communities in sedimentary and even igneous rocks over 2 km already available: not just species lists (http://www.sp2000.org/), but

known fossils. The palaeontological record indicates a Cambrian explosion of phyla around 540 million years (Myr) ago, but a sequences suggest a more gradual series of splits around twice as old23. Likewise, many orders of mammals and birds are now thought to have originated long before the end-Cretaceous extinction24,25, which occurred 65 Myr ago and which was thought previously to have been the signal for their radiation. If the new timescale can be trusted26, these findings present a puzzle and a warning. The puzzle is the absence of fossils. Why have we not found traces of these lineages in their first tens or even hundreds of millions of years? It seems likely Hominidae that the animals were too small or too rare, with the sudden appearance in the rocks corresponding to an increase in size and rise to Pongidae 27 b ecological dominance . The warning is that current biodiversity is in a sense greater than we had realized. Major lineages alive today represent more unique evolutionary history than previously suspected — history that would be lost with their extinction. Old-World monkeys Analysis of the shape of phylogenies has shown that lineages have 28 New-World monkeys differed in their potential for diversification. Darwin had noted that species in species-rich genera had more subspecific varieties, and subtaxa within taxa are often distributed very unevenly29, as Fig. 2 melanogaster subgroup c illustrates for eutherian species. But these taxonomic patterns can be taken at face value only if taxa are comparable, which they may not be. For example, species-rich groups may simply be older, and it is clear that workers on different groups currently place taxonomic boundaries in very different places30 (Fig. 3). Phylogenies allow comparison of sister clades — each other’s closest relatives — which by definition are the same age. Time and again, species are distributed too unevenly for simple null models to be tested in which all species have the same chances of diversifying31,32. genus Scaptomyza What are the species-rich groups ‘doing right’? Many explanations fall broadly into two types. Key innovation hypotheses33 posit 40 30 20 10 0 the evolution of some trait that permits its bearers to gain access to Millions of years ago more resources or be more competitive than non-bearers. Examples include phytophagy in insects34 and high reproductive rate in mam- mals35. Other hypotheses focus on traits that facilitate the evolution Figure 2 Taxonomic boundaries are not comparable among major groups. a, Fourteen of reproductive isolation — speciation — without necessarily species in nine genera representative of cichlid fish in Lake Victoria. b, Seven species increasing the fitness of bearers. Sexual selection36 and range representative of several families in anthropoid primates. c, Thirteen species fragmentation37 are examples of this kind. These two types can be representative of a single genus, Drosophila. Figure reproduced from ref 30, with contrasted as ‘bigger cake’ and ‘thinner slices’ explanations, permission. although some traits may act in both ways (for example, body size38,39); another way to split them is to view diversity as ‘demand- driven’ (niches are waiting to be filled, and differentiation leads to also maps of the geographical ranges of species (http://www. speciation) or ‘supply-driven’ (speciation occurs unbidden, with gisbau.uniroma1.it/amd/homepage.html), information on conser- differentiation arising through character displacement). Statistical vation status of species (http://www.wcmc.org.uk), bibliographies testing of many key innovation hypotheses is hampered by a lack of (http://eteweb.lscf.ucsb.edu/bfv/bfv_form.html), data on molecular replication — often, the trait in question is unique, and all that can sequence (http://www.ebi.ac.uk/ and http://www.ncbi.nlm.nih.gov/ be done is to model the trait’s evolution to assess how well it fits the Genbank/GenbankOverview.html), data on phylogenetic position scenario40. When characters have evolved multiple times in (http://phylogeny.arizona.edu/tree/phylogeny.html and http:// independent lineages, sister clades provide automatic matched pairs herbaria.harvard.edu/treebase/), information on the stratigraphic for hypothesis testing (although other phylogenetic approaches are range of species (http://ibs.uel.ac.uk/ibs/palaeo/benton/ and also available41,42). Comparing sister clades (the procedure used in http://www.nceas.ucsb.edu/~alroy/nafmtd.html) and much more. most of the examples above) avoids two problems that otherwise Although the terabytes of information already stored constitute only cloud the issue. First, taxa may not be comparable (Fig. 3), and a small drop in the ocean, the next two sections show how much can second, they are not statistically independent — related clades be seen in that droplet about the distribution of biodiversity among inherit their traits from common ancestors, so are pseudorepli- evolutionary lineages and through time. cates43. Nonetheless, there is ongoing debate about the role and limitations of phylogenetic tests for correlates of species Learning from the tree of life richness44,45. The ongoing explosion of phylogenetic studies not only provides an ever-clearer snapshot of biodiversity today, but also allows us to make Temporal patterns in biodiversity inferences about how the diversity has come about19–21. (For an Is biodiversity typically at some equilibrium level, with competi- ecological perspective, see review by Gaston, pages 220–227.) Phylo- tion setting an upper limit, or do mass extinctions occur so regular- genies give key information that is not available from species lists or ly that equilibrium is never reached? And, with one eye on the taxonomies. They detail the pattern of nested relationships among future prospects for biodiversity, how quickly does diversity species, and increasingly provide at least a rough timescale even recover from mass extinctions? Palaeontologists have addressed without reliance on a molecular clock22. These new phylogenies are these questions at many scales, from local to global. For the global pushing back the origins of many groups to long before their earliest view, the data come from huge compendia of stratigraphic ranges of

214 © 2000 Macmillan Magazines Ltd NATURE | VOL 405 | 11 MAY 2000 | www.nature.com insight review articles taxonomic families (see, for example, refs 46, 47), led by Sepkoski’s highlights the difficulties of taking taxonomic patterns at face ground-breaking efforts, and made possible by the development of value. Neontologists may face much the same problem with species: computer databases. There are more families now than ever before, taxonomists tend to recognize bird lineages as species if they are and a model of exponential growth provides a good overall fit to the older than 2.8 Myr but not if they are younger than 1.1 Myr (ref. 52), numbers of families through time, suggesting expansion without so apparent logistic growth in species numbers through time limit and no major role for competition in limiting diversity48. But a within bird genera53 might be expected even without a slow-down significantly better fit is provided by a set of three logistic curves, of cladogenesis. each with a different carrying capacity, punctuated by mass extinc- The patchy nature of the known fossil record means that some tion events49. Leaving aside the thorny issue of multiplicity of tests taxa in some places at some times can be studied in much greater and the big question of why the three carrying capacities are differ- detail than is possible for the biota as a whole. Studies at these ent, there may be a perceptual problem at play here. Families do not smaller scales can analyse the record at the species level, within a arise overnight: they are the result of speciation and a lot of time. region or biome, and can better control for problems such as incom- Consequently, exponential growth at the species level might appear plete and uneven sampling54,55. Such studies find a range of answers: like logistic growth at higher levels50. This problem of perception is communities may show an equilibrium diversity55,56, an increasing a recurrent one in palaeontology. For instance, good evidence that geographical turnover57, or radiation punctuated by mass extinc- biodiversity is often near equilibrium comes from the fact that tion58. This may be a more appropriate spatial scale at which to look extinction events are commonly followed by higher than normal for equilibrium, as the units have a greater chance of interacting59. rates of diversification4. However, the peak of origination rates of The temporal pattern of disparity is also of great interest. Does genera and families is not straight after the extinction peak. Instead, difference accumulate gradually and evenly as lineages evolve their there is a 10-Myr time-lag throughout the fossil record, implying a separate ways, or is evolutionary change more rapid early in a lag phase before diversification occurs51. But could the same pattern group’s history, as it stakes its claim to a new niche? Information arise if speciation rates rose immediately in response to the extinc- from living and fossil species and phylogenies can be combined with tion, but the new lineages are given generic or familial rank only statistical models41,60,61 to answer this question, although so far rela- after being around for some time? This scenario would predict tively little work has combined palaeontological and neontological (incorrectly) that family diversification rates would take longer to data. Rates of morphological and taxic diversification are often respond than generic rates, so cannot be the whole story, but it incongruent, or even uncoupled61, again highlighting that there is

a 2,000

1,500

b 1,500 1,000 Species richness

500

1,000

c 0 60 Sirenia Cetacea Primates Rodentia Pholidota Xenarthra Carnivora Pinnipedia Chiroptera Insectivora Scandentia Hyracoidea Species richness Dermoptera Artiodactyla Proboscidea

500 Lagomorpha Tubulidentata Macroscelidea 50 Perissodactyla Order

0 30 Gliridae Muridae Caviidae Sciuridae Pedetidae Dipodidae Zapodidae Castoridae Hystricidae Geomyidae Echimyidae Dinomyidae Species richness Seleviniidae Chinchillidae Bathyergidae Ctenomyidae Aplodontidae Capromyidae Abrocomidae Petromuridae Octodontidae Anomaluridae Heteromyidae Erethizontidae 20 Dasyproctidae Myocastoridae Thryonomyidae Hydrochaeridae Ctenodactylidae Family

Figure 3 Subtaxa within taxa are often distributed unevenly. Uneven distribution of 0 species among: a, eutherian orders, with rodents being the dominant group; b, rodent Genus families, with murids being dominant; and c, murid genera. Data from ref. 95.

Figure 4 Species richness in major groups of organisms. The main ‘pie’ shows the species estimated to exist in each group; the hatched area within Chordates each slice shows the proportion that have been formally described. Data Plants from ref. 7. Molluscs

Crustaceans

'Protozoa'

Insects

'Algae'

Arachnids

Nematodes

Fungi

Viruses

Bacteria

Others

more to biodiversity than numbers of taxa. At present, it is hard to extinctions, is highly non-random73–76, with related twigs on the tree tell under what circumstances disparity precedes, or perhaps drives, tending to share the same fate. This selectivity greatly reduces the species richness, and when the reverse applies. Different models can ability of the phylogenetic hierarchy to retain structure in the face of give very similar patterns of diversity and disparity over time60, and a given severity of species extinction77,78. detailed studies at smaller scale62,63 may provide the greatest chance But how much structure is needed? Imagine if the only function of of an answer. this article was the transfer of information. Many of the words could be deleted and you would still get the message. It would (we hope) be The shrinking biosphere less pleasant to read. Similarly, for many people we need biodiversity What about human impacts on biodiversity? A simple calculation because we like it; it should be conserved just as we conserve Mozart shows that recent rates of species losses are unsustainable. If there are concertos and Van Gogh paintings79. But how many words could you 14 million species at present7, then each year the tree of life grows by delete before the meaning starts to get lost? Recently, ecologists have an extra 14 Myr of branch length. The average age of extant species is begun asking similar questions about our environment. nearly 5 Myr (in primates and carnivores anyway, and species in most other groups probably tend to be older rather than younger). So the Biodiversity and the stability and functioning of ecosystems tree can ‘afford’ at most about three species extinctions per year How many species can we lose before we start to affect the way ecosys- without shrinking overall. There have been roughly this many tems function? Principal environmental factors such as climate, soil documented species extinctions per year since 160064, and most type and disturbance80,81 strongly influence ecosystem functioning, extinctions must have passed us by. The rate has been increasing too: but likewise organisms can affect their environment82. Some of the the last century saw the end of 20 mammalian species alone, a first ideas on how biodiversity could affect the way ecosystems pruning of the mammalian tree that would take at least 200 centuries function are attributable to Darwin and Wallace28,83, who stated that a to redress. diverse mixture of plants should be more productive than a mono- Estimates of current and future rates of loss make even more culture. They also suggested the underlying biological mechanism: sobering reading. The rate at which tropical forest — probably the because coexisting species differ ecologically, loss of a species could habitat for most species — is lost is about 0.8% to 2% per year65 (call result in vacant niche-space and potential impacts on ecosystem it 1% for the purpose of this example). We must expect about 1% of processes. Defining ecological niches is not straightforward, but the tropical forest populations to be lost with it, a figure that may be Darwin and Wallace’s hypothesis, if correct, provides a general as high as 16 million populations per year, or one every two biological principle which predicts that intact, diverse communities seconds66. Most species have multiple populations, so rates of are generally more stable and function better than versions that have species loss will obviously be much lower. They are most commonly lost species. Recent experimental evidence (reviewed by Chapin et estimated through species–area relationships65, although other al., pages 234–242, and McCann, pages 228–233), although pointing approaches are used too67. Wilson68 famously used the species–area out important exceptions, generally supports this idea. Compared relationship to estimate an annual extinction rate of 27,000 species with systems that have lost species, diverse plant communities often — one species every twenty minutes. This and similar estimates have have a greater variety of positive and complementary interactions attracted criticism but recent work67,69,70 has shown that levels of and so outperform any single species84,85, and have more chance of species endangerment are rising in line with species–area predic- having the right species in the right place at the right time. This last tions, provided the analysis is conducted at the appropriate scale. ‘sampling effect’ mechanism has prompted much debate on the What are the implications of such rapid pruning for the tree of life? design, analysis and interpretation of experiments that aim Simulations in which species are wiped out at random71 indicate that to manipulate biodiversity86. Although the sampling effect is most of the phylogenetic diversity would survive even a major biological in part — it requires both differences between species and extinction: up to 80% of the branch length could survive even if 95% an ecological mechanism making some species more abundant than of the species were lost. This result assumes extinction to befall others — the probabilistic component (more diverse communities species at random; scenarios of non-random extinction can have have a greater chance of containing a species with particular proper- very different outcomes72. The current crisis, like previous mass ties) has made it controversial. Nevertheless, loss of species with key

Box 2 Plant diversity and productivity at different scales Diversity Latitudinal gradient

Productivity Diversity

Biomass gradient

Productivity Diversity Productivity Experimental diversity gradient

Diversity Productivity

For plants, the relationship between diversity and productivity productivity increases. Experimental manipulations of plant diversity changes with scale107,108. At global scales (panel a in the figure within habitats (c) reveal that, although relationships vary, productivity above), from high latitudes to the tropics, plant diversity in large areas tends to increase with diversity owing to increasing complementary or may be positively related to increasing productivity. At regional scales positive interactions between species and the greater likelihood of (b), plant diversity in small plots is frequently negatively related to diverse communities containing a highly productive species. In increasing productivity, often as part of a larger unimodal ‘hump- manipulation experiments, biodiversity is the explanatory variable and shaped’ distribution of diversities. Numbers of species correlate with productivity the response, whereas in observational studies the several factors including the size and hence number of individual relationship is usually viewed the other way round as illustrated here plants sampled, spatial heterogeneity, and competitive exclusion as for all three cases. traits, as in the sampling effect, is not restricted to ecological experi- agreement and differences in experimental results. Nevertheless, this ments: logging, fishing, trapping and other harvesting of natural work represents only a first general approach to the subject; many resources frequently remove particular organisms, often including issues remain outstanding and other areas are as yet uninvestigated. dominant species. First, do these short-term and small-scale experiments in field plots Although 95% of experimental studies support a positive reveal the full effects of diversity, and how do we scale up in time and relationship between diversity and ecosystem functioning, many space92? Second, although we know that local extinction is often not have found that only 20–50% of species are needed to maintain most random, many recent experiments compare the performance of biogeochemical ecosystem processes87. Do the other, apparently communities differing in the presence or absence of a random set of redundant, species have a role to play over longer timescales, provid- species. How adequate is this model? Third, how will species loss ing insurance against environmental change? We need to know. interact with other components of global change such as rising CO2? Biodiversity can also impact ecological processes such as the inci- Darwin and Wallace observed that niche differentiation could cause dence of herbivory and disease, and the resistance of communities to changing diversity to have consequences for ecosystem processes, but invasion. Once again, although exceptions exist, in experiments the magnitude of these effects could depend crucially on the exact which manipulate diversity directly, communities with more species mechanism of coexistence. Finally, how do we integrate these new are often more resistant to invasion88,89, probably for the same reason within-habitat relationships between diversity and ecosystem that they are more productive. Diversity of one group of organisms processes with large-scale patterns in biodiversity and environmen- can also promote diversity of associated groups, for example between tal parameters, as reviewed by Gaston on pages 220–227 of this issue? mycorrhizas and plants90 or plants and insects88. Box 2 suggests one way in which the relationship between plant The study of the relationship between biodiversity and ecosystem diversity and productivity could vary with scale. processes has made rapid progress in the past decade, and is proving an effective catalyst for linking the ecology of individuals, communi- Challenges and prospects ties and ecosystems. Some general, although not universal, patterns Recent years have seen exciting advances in our knowledge of biodi- are emerging as theory and experiment progress together91. We have a versity, our identification of factors that have shaped its evolution good understanding of the underlying causes, where we see both and distribution, and our understanding of its importance. But we

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remam >1000 years old have been sexed using a We believe that our recommendation ef Agricdturai Sciences, Box 597. slmlar techmque;) at ambient temperatures. PCR~based techniques for avian sexing was S-751 24 Uppsala, Sweden All of these are important considerations for the based on objective cnteria which would be most molecular ecologist who may not have access to useful to ecologrsts embarking nn such a project. spaaaltzed means of sample collectron and storage The reader may assess our objectrvlty by while m the feid. or who (nay have collected enaminrng their nearest laboratory for the Dept of Zoolo~~, Uppsala University, samples for other ~LIIOOS~S.but now wheS to presence of a PCR instrument or a flow cytometer Villavageri Y, S-7.52 36 Uppsala, det~lmk? tk SEh 17: i!‘W mdlvi@Ja~S. ~OreoL’er. in If neither IS available. but a means for reliable Sweden this specific case a unrwersal protocol for avian sexmg of birds IS required. the chotce may be sexing Involving only PCR and electrophoresls IS between purchasing a flow cytometer which may likely to be available soon3-5. or may not be able to reveal the sex of the 1 Taberlet. P. etal. (1997) Mol. Ecol. 6.869-876 In contrast, flow cytometry is only applrcable to species of interest, or. for about one tenth of the 2 Faerman. M. et al. (1997) Nature385 212-213 bird species in which tile sex chromosomes differ cost, a PCR instrument that almost certainly will 3 Grifiths. R. and Tiwari. B. (1993) Proc. A&/. Acad. significantly in size. and even in these cases be able to and which will also be useful for Sci. U. S. A. 90. 8324. 8326 requires calibration using fairly large samples microsatellite genotyping, RAPD. mtDNA, MHC. 4 Grifiths. I?.. Daan. S. and Dilkstra. C. (1996: froc. of lndiwrdualsof known sex. This would. for instance. SSCP and sequence analysis, and numerous R. Sot. London Ser. E 263.1251-1256 limit the value of the technique 111studies of other applications In molecular ecology. 5 Ellegren, H. (1996) froc. R. SOL. London Ser. 8 endangered species”. Rnally, an attractive feature of 2G< 1635-1641 PCR teehn~qucs is that 111acldltlon to mforniatlon 6 Gnfflths. R. and Tiwarr. E. (19951 Nature 375 about Sex, tile IW2Sti@tQr WIII ~!dSiiy h’e %m?ss to 454 DIVA StXjtlC?llC~? iflfO~S,lCIt~Oll ihi 1121 lllli’,l1! ‘Ii’ ‘\ ii’illl’ i’ 7 Ellegren, H. and Frldolfsson. A-K. N?t Genet. m cvoitittonary or poprrlatlor !udles (,I” press)

anililals are well represented, whereas earlier parts of the Precambrian fossil record are incompletely known. A key criticism of the fossil record is that ii probably becomes worse the further back in time one goes”. Comparisons of independent data sets, and error modelling, suggested that the fossil record is not statistically significantly biased, at least at higher taxonomic levels (i.e. gen- ~a, fami%ies)Y.In a third approach, comparing changes in knowledge of the fossil record through research timex,“, biases !:nvc :‘ZrEc:! 6.X: to ‘GCdisli-ib”titl: 8 &it- tlomly with respect to geological time. Two further approaches, one geological and the other phylogenetic, have suggested that the fossil record is a as a representation of true pat global-scale diversification. First, compar- tionally well preserved fos- if? today is hugely diverse, with current been a criticism ~a~t~cu~ar~yof the use of in which soft-bodied as well estimates ranging from three million: fossils in phylogeny reconstruction’,“. The ied organisms are retained, to 50 million species’. It is likely that all enthusiastic palaeonttilogist might assert iiminulion in quality back knowa organisms originated from a singIL that fossils add information not available in through the Phanerozoic~“. The same is common ancestor, and it is of interest to extant taxa, that they offer ~~or~~~ologies true OI winnowed concentrations of know how this hu$e diversification hap and modes of !ife that are entirely unpre- marine shells (roquin: :)‘I. Secondly, and pened. In an ideal world, the best ap- dictable from modern forms, and that Ihey contrary to expectation, comparisons of proach to establishing the pattern of the fill gaping holes in phylogenies’. Fossils fossil record data E’ith morpho!;gical and diversification of life would be to collect also are datable, and they add the unique molecular phylogeniesS~‘2-i8 have shown data from a comprehensive fossil record dimension of time to all phylogenies and good agreement by ‘axonomic group, and to rend off Phc empirica pattern as diversification patterns’. Can these oppos- habitat and geological agel!‘“l’. ~ocu~~e~te~ by the fossils. The world, ing viewpoints be resolved? The fossil record us good enough to however, is not ideal, and this approach document aspects oft entails many problems of ~~ter~retat~o~~ and it can be assulred that errors an not feast the quality of the fossil record. In studying patterns of diversification. gaps are randomly distributed with Acrilic of the fossil record might assert ~a~aeo~tolog~sts typically focus on the respect to time. Following normal prac- that fossils are, by definition, less know- past 550 million years (Myr), the Phanero- tice in ~a~~~~~l~~~~~~/, ‘diversity’ is able than extant organisms, and hence zoic (literally, ‘abundant life’). or the Ven- assessed simply as numbers of species, should be accorded a secondary role in dian (610-5SOMyr ago) plus the Phanero- genera or famiiies, as indicated, and gen- interpreting patterns of evolution. This has zoic. During this time, multicellular erally on a global scale. sectors of fife through time. nor on whether he dissected intosuccessive radiations of go from one al9 patterns of diversification adhere to major tetrapoo groupsl” - basal tetrapods species to many (Fig. l), and these include the same model of increase. However. the and synapsids. dinosaurs, and birds and three simple mathematical models, linear, choice of model is important since each mammals - but none of them shows a Eo- exponential and logistic, each of which has makes profoundly different claims about gistic pattern. The pattern of diversification attracted some attention. These are shown evolution. of insects (Fig. 2d) is also largely exponen- first as ideal uninterrupted models (Fig. la), tial, especially in the last 100Myr, but could and second with some mass extinctions be said to be approaching an equilibrium superimposed (Frg. lb). level now 31. The linear modePJ’ represents net Recent plots of the diversification of additfve increase, simply the addition of a invertebrate families (Fig. 2a) shows a families of marine, conlinentaf and ‘ah’ life fixed number of new species in each unit of short pfateau in the Cambrian (c. 40 Myr), (Fig. 3) founded on a new data base:“‘, time. En terms of an evolutionary branch and a longer one from the Ordovician to the confirm these varying models for diver- ing model, additive increase would mean Permian (i. 250 Myr)Z~,This is followed by a sification. The continental curve that, through time, speciation rates have long phase (250 Myr) of n tial dominated by tetrapods, insects and land declined, or that extinction rates have in- increase in diversity throu Ok plants, is exponential. The marine curve creased regularly at a rate sufficient to mop and Cenozoic, the rising element of a third (Fig. SC) has been explainedZHby two fogis- up the excess speciations. The exponen- logistic CWW, VJhkh ShOWS a hht Of a S~BW- tic curves, one in the Palaeozoic, and the tial madeW’ is more understandable in down in the last 25 Myr or so, suggesting second in the post-PaPaeozoic, with the be- terms of a branching model of evolution. that a third plateau level may be achieved ginning of a plateau phase in the Late Mio- If speciation and extinction rates remain 125 Myr in the future?“. ceno or Pfiocene, some 5-10 Myr ago. The roughly constant, then there will The diversification of species of vascu- con~irination of all marine and continental far doubling of diversity within fixed units lar plants (Fig. Zb) has been interpreted in families (Fig. 3a) can be explained by a sin- of time. The logistic model’“-“’ involves a similar way”!t,:11’with a model that involves gle poorly fitting exponential curve. one or more classic S-shaped curves, each the successive rise of new major bauplane There may be ~~a~~~~~~~~~e~~ti~~differences consisting of an initial period of slow di- of plant types -early vasculihr plants in the between marine and continental life. Rates versity increase, a rapid rise, a slowing of Devonian, lycopods, ferns, conifers and of taxonornic turnover in marine inver- the rate of increase as a result of diversity- others in the Carboniferous to Permian, tebrates declined through the Phanerozoic dependent damping factors, and then a gymnosperms in the Triassic to Jurassic, after the initial rapid Cambrian radiation. plateau corresponding to a limiting or equi- and angiosperms from the Cretaceous on- while vascular land plants show increas- hbrium value. wards. The initial segment of the curve is ing rates of turnover through time”. Ter- There is no consensus on which model logistic, but the later segment is fit equally restrial vertebrates show intermediate pat- best explains the diversification of major by a linear or exponential curve. The diver- terns Perhaps adaptive space was filled sification of continental tetrapod families early on in the sea, while land plants (and (Fig. 2c) is best explained by an exponential possibly vertebrates) have continued to curve. The pattern of diversification may conquer new ecospace, and may still be

r (a) I

1 500 400 300 200 100 0 Geological time (Myr)

600 400 200 0 Geologrcal hme (Myr) Geologtcal time (Wlyr)

(d fd) 600’ L!l Non-marme tetrapods 1 5 400. ,m B FJ n L? zoo- & z’

Geological time (Mya)

Fig. 2_ Theoretical models for the diversificatior Geological bme (Myr) Geological tnne (Myr) of life. (a) In the absence of maJor perturbabon and (b) wrth two mass extinctions supenm Fig. 2. Patterns of dtversificatron of (a) faInrIles of marrne Invertebrates, lb) VdYLUkX land plants. (C) 11011 posed In each case, the upper curve IS the marme tetrapods and (d) Insects. Abbrevratrons: C. CambrIan; Crb. Carborrlferous: Crrl. CretacWW. lcgistic or equrlibnum model. the middle curve D, Devonran: Jur, Jurassic; 0. Grdovrcran: P, Penman: S. Srlurran: Ted Tertary: Tr. Trrassrc. V. Vendran. is the addittve or straight-line model, and the Eased on Refs 9. 19. 30 and 31. lower tune IS the exponential model. i ponential models; however, this would be clade competition has often been assumed, restrictive, not feast since the early phase without being precisely defined, but this of a logistic curve is typically exponentiaf. viewpoint has been questioned”,““-l’). A The key distinction is between equilibrium second view is that interspecific compe- and non-equilibrium (expansion) models. tition can scale UQ to be expressed at higher Equilibrium models imply the existence of levels’;. Patterns of waxing ahd wanimg of global equilibria in diversity, while expan- the clades are attributed to diffuse com- sion models assume that there is no ceil- petition between members of species being to the diversity of life, or at least that longing to the different ciades, where spe- such a ceiling has yet to be reached. cies in clade A are generally competitively superior to their ecological analogues in Equilibrium models clade B. 03 600 500 460 300 200 100 Q Equilibrium models for the expansion A critical assumption of logistic mod- 1600 of the diversity of life developed from an els is that equilibrium levels exist - steady .B 1400 influential body of ecological theory that state diversities at which speciation and z 1200 explained species assembly in confined extirction uaees are $a\ance 22 1OOQ patches of living spat+. This island-scale the c3se of global diversification patterns, z 8Oil model these limiting prcc.esses could affect both $ 600 was extended’“.“5to regional and extinciivn and origination rates”‘, but 5 400 global scales, so that the island became z 200 ocal rates of colonization origination rates may be more diversity- 0 came global rates of origi- dependent”‘. However, there is no inde- nation and extinction of species. Time- pendent evidence for equilibria (i.e. for scales moved from tens or hundreds of fixed carrying rapacities)4’,4:i. In evofution- (c) 600 500 400 300 205 100 0 ycan-s to millions. ary terms, equilibrium diversities imply 1200 Logistic modelling of global-scale data that 411avaiiablc resources are in use. How- Iii 1000 on diversification implies (1) interactions ever, with enough time, and with normal E 800 among species within ciades, (2) interac- rates of origination and extinction, certain ; 600 tions between clades and (3) global equr- new species can surely insinuate, that is, iibrium levels. Many studies show that find new things to do, and thereby increase 2 400 ciades may radiate initially at exponentfal species diversity with almost no limit 1-1.1s. z’ 200 rates, and then the rate of diversification 0 slows at a certain point as a result of some Expansion models diversity-dependent phenomeno Ciades do not all diversify in the same Geological time competitive exclusion, increase way. Some radiate rapidly, reach a maxi- packing or reduction of species mum size, and remain at that diversity Fig. 3. Patterns of We diversification of lrfe through time, plotted for (a) all organisms, This style of reasoning follows explicitly Ievel until they become extinct. Others con- tb) continental organrsms and {c) marine or from classical experiments in competition tinue for long spans of time at low diversity ganisms. in terms of changes m numbers of where the increase of one population sup- levels, and some, such as insects, angio- famriies extant per stratrgraphic stage. In each presses another population that depends sperms, birds and mammals, seem to con- graph, a maxrmum and mrnimum is shown, tinue based on a combmation cf stratigraphic and on the same limiting resource. radiating linearly or exponentially habrtat preference rnf-?rmatron. The minimunr The pattern of diversification of marine for many tens or hundreds of millions of measure mcludes only families recorded as families (Fig. 2a) has been interpreted?” in years. Perhaps life diversifies in this way, definitely present withm each siratigraphic terms of a three-phase logistic mode) which with communities maintained well below stage, or as definitely spanning that stage, and represents the behaviour of three evolu- any resource limitation”Z3”s~“6. only rdnrii~eb &hg,;dted as rcstrictcd solely t3 the marine or continental realm. The maxmum tionary ‘faunas‘ (Fig.3): Cambrian, Palaeo- ‘We overall pattern consists of the sum measure rncludes also all doubtful stratigraphic zoic and Modern. The Cambri of diversification behaviours of n attnbutrons of families, and all equivocal and sisted of organisms with bro unrelated cfades. In the past 250 shared habitat designations. The sum of mmi- and trophic requirements, w diversification of life has been dominated mum measures for continental and marine orgamsms is equal to the mmimum measure Palaeozoic groups included more special- by the spectacular radiations of certain for all taxa together, but the sums of maximum ized forms. The Cambrian generalists were clades both in tbr sea (decapods, gastro- medSUreS do not equal the maximum measure able tu radiate rapidly at first into empty pods, teleost fishes) and on land (insects, for all taxa. because famrlies v&h equivocal ecospace, but because of their lack of spe- arachnids. angiosperms, birds, mammals). envrronmental assrgnments, and those which occur rn both manne and continental settings, cialization could not reach high diversities. The rate of increase has been exponential are counted as both marine and contrnental. New more-specialist forms could subdi- in the case of families of continental organ- Cen. Cenozoic: PC. Precambrisr,; other abbrevi. vide the ecospace more finely, an atrons as for Prg. 2. Bxed on Ref. 24. achieve higher diversities. The lModern rine families Gigs 2-4). Such expanding, ~-- evolutionary fauna, characterized by new even exponential long-term diversification predatory groups and new defence strat- patterM may be understood intuitively. continuing to do so. ~~ver$~ficatio~ on I egies, was apparently able to achieve yet For example, the evotuti began later than in the sea, and new gro higher diversity, (Fig.5a) was characterized of plants invaded unstable habitats and There are two views of the evolution- unpredictable, expansio modified them”“. ary interactions oi species and higher taxa. from fresh waters to la Oneview is that cfades compete in abroad- burrowing underground, rxcupying hu-

scale way. In other words, a newly arising man habitations . . . Who is to say what new clade, or an invading group. is regarded as habitats or modes of life vertebrates may r the diversification competitively superior to another and can adopt in the future which will drive their of fife cou!d be compared solely with ex- thereby replace it wholesale. Such inter- diversity ever higher? - -

afterthis initiai expunentiai rise’“. This strongly suggests a logistic/equilibrium explanation. (2) The aadiation of life OPTland, and 0P certain major marine and Co~~t~Re~ta~ ctades, appears to have LolPowedan exponential pattern, and there is IPOsign of slowing down in the rate of increase, nor cf the occurrence of any e~~~l~br~~~~levels. These radiations strongly suggest patterns of unfettered expansion. (3) There were rapid rebounds after mass extinctions, in which local and global diversity recovered to pre-extinction levels during relatively short spans of time This suggests that ecospace that had been vacated as a result of an extinction event could refill at a higher rate than entry into new ecospace. Such rapid rebounds suggest a logistic/ equilibrium model of diversification”. They could also be un Fig. 4. Dlverslflcation of manne mverts9rates. and the three ‘evolutionary faunas’, Cambrian (tillobltes inartlctiiate brachlopods. monopiacopilorans. hyolrths), Palaeozorc iartrculate brachlopods. crinords in a world of unfettered expansion, es- rSzphalopods. stenolaemate bryozoans, non-scleractinian corals) and Modern (bivalves, gastropods. echln pecially since most rebounds reached lev- uii?c, chellostome bryozoans. malacostracans. scleractcnian corals. fishes). Abbrevlatlons as fcr FIN 2 els that were higher than pre-extinction. Based on Refs 2 1 and 25. (4) Late phases of d~v~rs~f~cat~o~cycles i 1 are associated with declining rates of origination and increasing rates of extinction, Exponential increase could imply that as the logistic curve approaches the equi- di,versification would last for ever. Presum- librium level. The marine record generally ably there is an ultimate limit to the num- The five following observations may confirms such expectations. and provides bers of families, or ot er taxa, that can in- provide test cases for dist~ng~isbing be- evidence for the logistic modeF. habit the Earth at any time”‘: such a limit tween equilibrium and expansion models (5) The Palaeozoic pla: eau in mark? would be caused not least by the amount of the diversification of life: animai diversity is stron, evidence for of standing room on the Ark, and ulti- (1) There was an evolutionary explo- equilibrjum’i’i,:‘“. mately the availability rofthe chemical com- sion of marine animals during the early All five points require !:l!‘i.er study. but ponents of life, principally carbon. Cambrian, and diversification rates slowed only the last two will be e?$lored further

Age (WrJ Age Pbr) (4 400 350 300 250 20O 150 100 50 0 400 350 300 250 200 150 IOC~ 50 0 70

All tetrapods - 60 cumulative totals 50

40 Maximum CCRs

Geological time GeologIcal time

Eg. 5. (a) Dlverslficatlon of tetrapod famrlies through time, and(b) thelr styles of ongmation. Data are from Ref. 32, and are based on all 840 non-singleton famllles of tetrdpods. A total of 194 smgleton families were excluded, those that are currently based on single spectmens or single spec:es from single localltles. ln (h). all ongmabons of tetrapods of all habitats are shown, as well as overlaps and maximum candldate competlt!ve replacements (CCRsj. CCRs were identrfred by comparrson of Pairs of famllres. First, stratlgraphlc range charts were Plotted for each combination of body size. diet and habltat. and maximum geographic ranges of each famllY were noted. Then, the Point of ongm of each of the 840 families was scrutinized to determine whether it was a CCH or an expansfion. CCR cases were subdWed Into overlaps, where the stratIgraphIc range of the family overlapped another family, and situatrons Were the family apparently onginated at the Precise time of eWIctlon of another (gap 0), or after a gap of one or two (gap I. 2) stratIgraphIc stages. Overlaps grve evrdence that the two familtes could have encountered each other. while the gap 0, 1, and 2 cases SNOW for possible incompleteness of the fossll record. CCRs are plotted as overlaps and maximum CCRs (the sum of all overlaps and gap O. 1. and 2 cases), Abbreviations as for Fig. 2. Basedon Ref. 48.

_- - - tetrapod niches w<:refilling up at either of obvious whether life has yet reached the global taxic carrying capacity. (3 those times. The most telling evidence for equilib- 200. Orders rium modeis of the iong-ternr diverGil- cation of life is the Palaeozoic ‘plateau’ in ~May.R.M. (1991)) Hovi maray species? Pl~rlos ,//----bT marine invertebrate diversity (Figs 2a, SC, PO/IS I< Sot London Ser. K 330, 293-304 ,001 4). This has been interpreted in a number I’ntterso!l, C. (1981) §~~~~~~~e of foS§ils in of ways. ~~~~~~~~~g evolutionxy reelatioosbips, (1) “It is rtti! and indicates a global limit nnnu /hi !?o/ .5j!st 12. 195-223 oL-- to diversity’. According to this view25,2i,:ti, Goodman, M. (1989) ~ergiog,~t~i~ce of the plateau is sustained at a total level of ~~yfoge~e~c systematics sod moixular biofogy: A new age of exploration+ ih about 550 families,composed mainly of the Families The Hierarcig ofLife (Fernhokn, B.. Bremer, K. equilibrium diversity of 350 families of the and Jornvall, H., eds). pp. 43-61. Elsevier Palaeozoic evolutionary fauna. Smith, A.B. (1994) S_Wernoticsand the Fo.sbssil (2) ‘It is real but was maintained below Record. Blackwell Scientific any maximum carrying capacity by per- Renton. M J. (i99.5) Testing the time axis qf turbations’. According to this view, per- ~~~y~Q~e~~es, Plrrios Trms R .Soc London turbations have kept communiti@- well ser H 348. S-10 helow any reao~rg-e ]imitation"",'".4',4~~.4~,~~,Raup, D.M. (1972) Taxonomic dive&y duriog e Pha82erozoic, hence 177 IOf&1071 and the quality of fit of some of the models to the data is claimed to be as good as nton, M.J. (1987) The of the biosphere: e~~~~~~~~~ o-e~u~~ib~ [email protected] number of kinds of models of global diversity, Trends Ecol. Er non-eq~~l~br~urnmodels have been pro- 2.153-156 posed, some that are broadly diversity- Maxwell. W.D. and Bento,i. M.J. (1990) dependent?‘;, others in which speciation Historical tests of the absolute completeness is diversity-dependent, but extinction is of the tossil record of @etrapods,Poleobrolo,qv diversity-independent~~~Q4~.and finally a 16.322-335 neutral model that assumes random and Sepkoski. J.J., Jr (1993) ‘Fen yem in the lih~aq: how changes in taxonomic data (d) independent variation in lates of speciation and extinctionZZJ”. erception of ~ac~~evQ~~l~0~~ 1 CO% ppttenn, PaCobiolo~ 19,43-51 Species (3) ‘It is an artefact of taxonomic lev- 1 I els’. A final view could Se that the plateau A.;ison, ?‘.A. and Briggs, D.E.G.(1993) ~~~e~~~~~ fossil recorrd: d~s~~~t~o~ of is an artefacl of analyses carried out at high sc-f&tissue ~~rese~~at~o~ taxonomic level. A comparison of plots of ~i~~erozoi~, WJ/O~ 21.527-KS1 the diversity of marine life through time I:rdwell. S.M. c11ci Brrnchley, P.J. (1’196) EvobraiorP 3: the fosd ~recor& 600 400 200 C at ordinal. familial, generic and s level (Fig. 6) shows how the logistic pat- lrijids in marine skeield ~~c~rn~~~~~s and Geological time (Wlyr) tern appears to decay into an exponential their i~~~~ca~~~s, in Evolutionor?, pattern. At ordinal level. there is a single 1’ukwo6to~o,g_y (Jablonski, D.. Erwin, D H. and Rg. 6. Patterns of dIveI siilcatlon of well-skeleton long plateau, at familial level, the shorter Lipps. J.H.. eds). pp. 290-336, University of lzed marine animals. counted as ia) orders. (‘hicago Press (b) farnilles. (cl genera and id) species. The Palaeozoic plateau. At generic level, the Palaeozoic plateau is present”!‘, but it is Norell. M.A. and Novacek. M.J.(19Y2) ordinal, fam&al. and genenc counts ure based fossil record and evolution: compari on empirical data, while the species curve is relatively lower than the familial teau, clad&tic and ~afeo~to~ogic evidence for based on real cour.ts and on simulations. Based and the post-Pakewzoic divers% on of vertebrate B&tory, Science 255,1690-1693 on Refs 25, 9.119 and 50. respectively. genera is more exponential in appearance. Benton, M.J. (1994) ~a~~e~~~o~og~~~ data, an For species, there is a;roavaiiabie empirical i~~e~t~~~n~ mass cxtioetions, Trends Ecol curve, but a suggested co Euol. 9, 181-185 here. The slow-down in diversification retains indications of a two rates as the asymptote is approached zoic dfvers~ficat~~npattern, but the pat- (point 4) is critical to the logistic model. tern on the whole is exponential. P At this time, there should be a switch in the nature of group originations, from ori- ecospace, to more and displacement of pre- existing taxa. An outline study of familial 1 models are more appro- originations of tetrapod#“H has provided priate than logistic. for tile diversifickon no evidence for the a of marine animals. Henton. iL1.J. and Hitchin, K. (1996) rium at any point (Fig. quality of the fossil record by gro ilies of tetrapods that have a fossil record, Co major Lab&&, Hut. fhol. 12. I1 l-157 13-2cP!%of familial origins couid be (but There is no doubt that competition oc- Benton, M.J. and Hitchin, R. ~o~g~e~ce need not be) exp?ained by competitive curs between individuals in populations of between yhylogenetic and s~~~ig~~~ic data with a pre-existing family.How- microbes in enclosed laboratory vessels, on the history of fife, bar. R. Sot. London Ser R (in press) istribution of peaks is random and between individuals in ~~~i~~a~~o~s on with respect to time. There is no evidu?ce Renton. M J 41985) #a+$ e~~~c~~~~ .amapng islands”“.However, it is not clear w%ther nona-marine Betrapods, Nulurf 316.811-814 for a rise in candidate competitive replace- such modefling can be extended to re- Jablonski, D. (1991) Extinctions ments in the late Palaeozoic or the late gional and global scales. The biosphere is a ~~eo~~~~o~~l~~ perspective,Science 253, Cenozoic, and hence no suggestion that essentially a closed system. but it is not 754-757 21 Walker, T.D. (1985) ~~ve~~K~a~~o~ 3 H. and Knoll. A.H. (1985) 41 Levinton. J.S. (19 theory 0T diveax@ functions an rate of ~~~~~rn~c e~~i~t~~~rn amt holo@caP evolution. ev~~~t~o~, in erozo,c Dfversr.?; Pdlerns sat&e Science 204. 335- Profdes in Macroevolutron (Valentine. J.W., species level, in Phanerozorc Divers@ Pootwms 42 Walker. T.D. and Valentine, J.W. (1984‘)/ ed.). pp. 31 l-234 Princeton University hofiles in Mucrvecolufion (Valentine, J.W d.) Press pp. 97-128, Princeton University Press 22 Hoifman. A. (1986) Neu 31 Lahandeira, C.C. and Sepkoski. J.J Jr (19%) ity in tie E0ssilrecord, Soerrre 43 Valeniinc. .j \k; (19%) A theory of otiginatiors ~a~~~ev~~~~t~~~, R! .lb Go1 PdOonf Abh Ii:! and ~x~~c~io~, in Ptlunerozoic L?icfw& 219-244 32 Benton. M.J. (1993) The Fossrl Record P. P~ltlerl-ls PdilC~\ ,n .3k,c_rrlrr~okltf;,:, 23 Cailleux. A. (1954) How many species? Chapman L Hall (Valentine, J.W., ed.), pp. 419-424, Princeton Evolution 8,83-84 33 Valentine, J.W.. Tiffney. 5.H. and University Press 24 Benton, M.J. (1995) ~~ve~t~cati~~ and Sepkoski. J.J.. Jr (1991) ~vo~~~~n~ dynamics 44 Wilson, E.O. (1969) The species e~~i~~~~~~~ e history of life, Science 268. ts andanimals, Palu~os6,81-88 Brookhaven Symp. Biol. 22.X-47 52-58 34 MacArthur, R.H. and Wilson, E.O. (1967) 45 Whittaker. R.H. (1977) Evolpltion of species 2; Sepkoski. J.J., Jr (1984)A kinetic model of The Theory 0llslandBfo~eo~raptgv. Princeton diversity in la& co unities, Euol 61ol. 10. Phanerozoic taxonomie divekty. 111.Post- University Press 1-67 PaEeazoie families and mass extinctions, 35 Rosenzweig, ML. (199.5) Species Di~rrsi~ 111 46 Hoffman. A. (1985) I&mad Pdeobiologv 10.246-267 Space and Time. Cambridge University Press jology: in sear& for evolutiormry 36 Gou!d. S.J. and Galloway. e~~~~~b~a~Biol. Rev 60.455-471 and ~~c~io~o~s - ships 47 Benton. M.J. (1990) The causes of the dynamics,in Phaflernzoic night, Pdeobiolog 6,383-39ii ~ive~i~ca~oQ of life, in Major Evolufionu~ Profiles m Macroecolulion 37 Bcnton. M.J. (1987) Progress and ~o~~e~t~o~ Rudiations (Taylor. PD. and Lanvood, G.P.. (Valentine, J.W., ed.), pp. 277-309. Princeton ia ~ac~evo~~~o~~ Biol. Rev. 62.395-338 eds). pp. 409-430. Ctarendon Press University Press 38 M.J. (1Y91) ~t~Ect~Q~, biotic $8 Benton. M.J. (1996) Testing the roles :G 27 Sepkoski. J.J.. Jr (1396) Cc upetition in men& and cl&e ~~te~ac~~~~s, in competition and expansifaonin tetrapod rnac~~~evotutio~~:tk double wedge @ ofEvolufionnty 8iolo.q (Dudley. L.C.. evdntiar., Proc K Sot London .+r R 2611, uevisatc;8, in Euolotionaq Poleohrolo,~, ed.) pp. 89-lO2. Dioscnrides Press ti4 1-tiMi (Jablonski, D.. Erwin, D.H. and Lipps, J.H.. 39 Lidgard. S.. McKinney. F.K. and Taylor. P.D 49 Sepkoski. J.J.. Jr (1996) Patterns of eds). pp. 211-255. University of Chicago (1993) Competition, c!ade replacement, and a iiactioaa: a perspective from Press history of cyetostome and cheilostome s, in Globul Events und Event 28 Courtillot, V. and Caudemer. Y. (1996) Effects bryozoan diversity, Pdeobiologv 19. liser, OH. ed.). pp. 35-51. of mass ex~~ctio~s on ~t~~ive~t~, :Vafuure 352-371 3X1.146-148 40 Eenton. M.J. (1996) Qn 29 Knoll. A tl. (1984) Patters o~ex~~c~on in ira species richness through time, in e fossA record of vascular plants, in tebqods, in Evolutionmy fakobiolog,v Phonerozoic Dwersr@ Patterns Aahlrs III E.~fincfroni (Nitecki. M.H., ed.). pp. 21-68. (Jablonski, D.. Erwin. D.H. and Lipps. J.H.. zds). .Mucroecoluiro~; (~‘aler~line. J.W.. ed,. Universit). .)f Chicago Press pp. 1X5-L’llJ. I’niverslty of Chicago Press pp. 129-150. Princeton University Press

------comparing and possibly testing the predic- ically unrealistic.’ Grammar is a prerequisite tions to see whether indeed the essence is not a guarantee for literature. captured in the model As Gillman and Bails clearly state, the) The best way to achieve a clear and un- wished to teach the grammar while intro- ambiguous formulation of the assumed es- ducing the literature. They have chosen to sence of ecological phenomena is to phrase present the mathematics piecemeal on a these in mathematical language not in the need to know basis and to use the didactic least because of great power to manipulate success formula of presenting separate is- by M. Gil/man and R. Hds the model once it has been framed in math- sues in boxes. Together they form a small Blacltwell Science, 1997. ematical terms. Because the mathematical 25page primer in mathematics where, step S19.95/$44.95 hbk (ix + 202 pages) model can easily be translated into compu- by step, the tools are developed: this can be ISBN 0 632 03(;34 6 ter language, this Qpens a wide field of read separately if so desired. They succeed manipulative/interactive exploration of the admirably in anticipating the mathematical he rationale for any model in ecology (or consequences of the formulated ideas. prolems and explaining them before they anywhere else) is the scientific desire to If one accepts this role for mathematics form a problem in following the ecological . . . . _, capture the essence and to remove or re- as the lingua lranca o! science then fnere argument, I have not seen a book in which duce the redundant aspects of the system is no alternative: ecologists should learn to this is done as carefully and as clearly as under study. What is essential and what is speak the language to bet+ communicate here. No need for students to be scared of redundant a. rLlereby what level of reduc- their science. This is not to ssy tlaat tse logic maths in eccJkJgy any more! It iS only b- tion is required, to a large degree depends ol the language is a guarantee for the qualii y wards the elld that the tight coupling on the questions being asked. The result is a of the c~~rnrnu~~cat~o~.As pointed out by between the ecological and mathematical modei’ of reality that is realistic to varying de Roes and Sabelisl ‘[spatial] models have argument begins to get lost. degrees. been shown to produce a bewildering vari- Given the wide variety of topics in ecol- A second reason for modefling is the fact ety of dynamical pher?omena to the extent ogy that are phrased in mathematical terms. that the abstraction obtained of rhe real that almost every corlceivable pattern can the authors had to select from the available world is much easier to handle and that we be generated by an appropriate model. Even models. Their choice seems reasonable: can ask of the model true Kantian ‘what if...’ worse, the assumptions of these models they choose for models with a high level of questions by changing the assumptions and cannot immediately be discarded as biolog- generality (i.e. high degree of reduction) and