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Challenges and opportunities in the measurement and assessment of biological diversity

Anne E. Magurran and Brian J. McGill

When we look at the plants and bushes clothing an entangled bank, we are tempted to attribute their proportional numbers and kinds to what we call chance. But how false a view is this! Every one has heard that when an American forest is cut down, a very different vegetation springs up; but it has been observed that ancient Indian ruins in the Southern United States, which must formerly have been cleared of trees, now display the same beautiful diversity and proportion of kinds as in the surrounding virgin forests.
Darwin, Origin of Species (1859)



By the 1800s naturalists had begun to document a fact that was surely apparent to the earliest humans: that species vary markedly in how common they are. Audubon, for example, noted that bird species in North America differ in abundance by up to seven orders of magnitude (McGill 2006; McGill et al. 2007). Darwins (1859) reections on the observation that some taxa are abundant yet many are rare, and that there are geographical differences in the abundances and types of species, shaped his thinking about natural selection. In drawing attention to the proportional numbers and kinds of species in nature, however, Darwin also identied questions that continue to challenge ecologists a century and a half later. Humans have a strong intuitive sense of the distinction between high diversity and low diversity assemblages, as encapsulated, for example, by the contrast between a tropical rain forest and a monoculture planted for timber. Moreover, the inequality

of species abundances that Darwin reported is so pervasive as to have acquired the status of an ecological law (McGill et al. 2007). However, quantifying the biological diversity of a community, assessing differences in this diversity over space or time, and doing so in ways that are useful to those who seek explanations for the natural patterns as well as to the managers and policy makers charged with the sustainable use of wild nature, is by no means as simple as it rst appears. The reason for this difculty is that biological diversity is a multifaceted concept that can be dened and documented in different ways. Being clear about exactly what we mean by biological diversity (or biodiversity) is the rst step towards measuring it. Even then the user can be confronted by a myriad measures, some of which will do a better job than others. The goal of this book is to guide readers through the entangled bank of biodiversity measures and provide an up-to-date and accessible account of this important and rapidly expanding eld.

1.2 State of the eld

2010 marks the United Nations International Year of Biodiversity (UN IYB), an initiative that highlights the growing need to provide informative and robust assessments of biological diversity. The objectives of the IYB are to promote the protection of biodiversity and encourage organizations, institutions, companies, and individuals to take direct action to reduce the constant loss of biological diversity worldwide. However, 2010 is also the target date set by the 2002 World Summit on Sustainable


Development for signicant reduction in the current rate of loss of biological diversity. It is by now generally accepted that the 2010 target will not be met, and of course there are many reasons for this, one of which is the ongoing debate about how best to measure biological diversity. The measurement of biological diversity has resonances with the parable of the blind men and the elephant where one felt the trunk, one an ear, one a tusk and another a leg, only to nd that they disagreed about the nature of the creature they had encountered. Quantifying biological diversity is in some ways like trying to measure an elephant (Nanney 2004). An elephant might be described in terms of its morphology or behaviour or neural circuitry, or DNA. Gene expression might be tracked through time or compared amongst individuals. The social interactions in different herds might also be explored. All of these approaches are valid, but clearly different. The investigator needs to specify which aspect of the elephant is being assessed, and then make the case that the types of measures adopted are employed correctly and are suitable for the purpose for which they are bring used. In the same way that there is no single method that entirely captures the essence of elephantness, so there is no one metric that perfectly quanties biological diversity. A large, and growing, number of diversity measures have been developed (Southwood & Henderson 2000; Royal Society 2003; Magurran 2004). Southwood (1978) (p. 421) wryly noted the explosive speciation of diversity indices and the habit of inventors of new measures to condemn their predecessors. Biodiversity assessment embraces not just the classical measures of richness, evenness, and species abundance distributions but also evaluations of occurrence, range size, and vulnerability as well as functional traits and phylogenetic diversity. It is clear that there can be no single best buy index that will suit all needs. Instead, clusters of measures have been developed to capture a certain aspect of biodiversity, with some of these performing this task better than others. Although it may seem like a disadvantage to have to choose amongst a range of metrics, the ability to examine biological diversity in different ways not only helps ecologists gain a deeper understanding of how ecosystems function, but also sheds light on

issues of practical concern such as the link between diversity and ecosystem services. The quantication of biological diversity probably began with Darwin, who in 1855 recorded all the plants in the meadow, Great Pucklands, next to his family home at Downe. His list ran to 142 species. It was over 50 years before the rst account of the relative abundance of species was published by Raunkaier in 1909. Other early, yet pivotal, papers by Motomura (1932) and Fisher (Fisher et al. 1943) laid the foundations for the investigation of species abundance distributions. Additional insightful and signicant contributions (including those by Preston (1948), MacArthur (1960), May (1975), Pielou (1975), Taylor et al. (1976), and Sugihara (1980) followed. These provide the framework within which biodiversity is measured, and still repay careful reading. Two developments that occurred towards the end of the twentieth century, however, shifted the measurement and assessment of biological diversity to a new gear. The rst of these was the recognition that biological diversity is a crucial global resource as well as one that is being lost at an accelerating rate, the second the advances in computing power that have fostered substantial improvements in statistical and modelling techniques.

1.3 What is in this book

Although vastly improved analytical and computing resources are of tremendous benet to ecologists, the rapid development of new methods, the inconsistent and sometimes confusing application of old ones, and the lack of agreement in the literature about the best approach means that users can be bewildered. This book provides an up-to-date account of the methods used to measure and assess biological diversity and places particular emphasis on the practical issues involved in measurement. It extends the discussion in Magurran (2004) and includes many new developments as well as a re-examination of familiar approaches. Our focus is measurement of the variety, abundance, and geographical occurrence of taxa, reecting the sense in which Darwin used the term diversity. The authors have wide experience of the measurement of biological diversity and have contributed to


recent advances. As bets a vibrant eld, our contributors do not invariably agree on which metrics and approaches are the best ones, although there is broad consensus about the essentials of biodiversity assessment. The various chapters set out the issues that investigators must consider and explain the advantages and disadvantages of different methods, thus helping the reader to reach a sensible conclusion about the best course of action in their own particular study system. The book is primarily aimed at those who need to measure and assess biological diversity. We have in mind upper-level undergraduates engaged in research projects, graduate students, and postdoctoral researchers, as well as environmental managers and conservation biologists. Although not designed as a theoretical ecology text, we nonetheless hope that the issues raised in the book will spark the interest of modellers and theoreticians. In each chapter the author(s) describe the state of the eld, discuss recommendations and future directions, and end with key points. The book begins with an overview of the basic measurement issues involved in biodiversity studies. As Scott Bonar, Jeffrey Fehmi, and Norman Mercado-Silva make plain, survey design and methodology play a crucial role in the success or otherwiseof biodiversity investigations. These are well-known concerns, although they often get much less attention than they deserve; Chapter 2 sets out the points that must be addressed before an investigation can even begin. In contrast Stephen Buckland, Angelika Studeny, Anne Magurran, and Stuart Newson highlight a problem that is potentially of great importance but one that has, until now, been almost entirely overlooked. Most diversity statistics proceed on the assumption that individuals and species have been collected at random from the community of interest and most investigators use these statistics irrespective of whether this assumption is fullled. In practice individuals and species often vary considerably in how easy they are to detect. Buckland et al. show how detectability can affect the conclusions drawn from diversity statistics, and provide advice on how to deal with the issues raised, although it is clear that assessing individual and species variation in detectability is easier for some taxa than for others.

The next section deals with the approaches that are sometimes described as measures of species diversity. Although the term biodiversity can mean many things, and is sometimes used in a generic way (EASAC 2009), most scientists, managers, and policy makers identify species richness as a central component. In many ways species richnessthe number of species in a given locality or assemblageis the iconic measure of biological diversity. It is used to identify biodiversity hotspots and plays an important role in conservation planning. Species richness also accords well with our intuitive sense of biological diversity. However, despite its wide appeal and apparent simplicity, accurate estimates of species richness can be remarkably difcult to achieve. This is not just at the global level, where it is still unclear, to within at least an order of magnitude, how many species inhabit the planet, but also at local levels and even for taxonomically well-characterized organisms. The reason for this difculty lies in the observations of Darwin and Audobonbecause most species are rare, an increase in sampling effort will almost always lead to an increase in richness. Fortunately there has been intense interest in recent years in providing solutions to this problem; Nicholas Gotelli and Robert Colwell provide a clear account of the approaches that can be used to make fair comparisons amongst sites where sampling effort differs (which can happen even if the investigator thinks that it is the same) and examine the new generation of non-parametric estimators that can be used to deduce the minimum number of species present in an assemblage. Although species richness is widely used as a measure of biological diversity, investigators often want to nd a means of quantifying Darwins proportional numbers and kinds in a single statistic. As noted at the beginning of this chapter all communities consist of species that vary in their abundance. However, communities (or localities) can also differ from one another in terms of their proportions of species, that is, in how even their species abundance distributions are. The degree of evenness can shed light on the processes that shape a communitys structure or provide a gauge of the impacts on it. There are a swathe of measures that populate the ground between species richness


and evenness. These include familiar choices such as the Shannon, Simpson, and Margalef indexes and a host of less well-known ones. Brian Maurer and Brian McGill explore this territory in Chapter 5 and provides guidance on the use of diversity statistics. Researchers may also want to go beyond an assessment of the diversity of a single site to say something about the larger picture. This might involve drawing conclusions about the distribution of biological diversity amongst a series of communities or examining sifts in diversity across a gradient. Whittaker (1960) rst made the distinction between diversitythe diversity of a site or habitatand diversitythe difference in compositional diversity between two or more sites. and diversity combine to give diversitythe diversity of the landscape. Until recently measures of compositional similarity and diversity received less attention than methods of assessing diversity. There has, however, been a marked increase of interest in this topic during the last decade and in Chapter 6 Lou Jost, Anne Chao, and Robin Chazdon provide an overview of this rapidly developing eld. The idea that the number of species recorded increases if a site is surveyed over an extended period has deep roots in ecology and was rst formalized by Preston. who argued that species area and species time curves are equivalent. The urgent needhighlighted by the UNs IYBto quantify changes in ecological communities and to determine whether the rate of biodiversity loss is accelerating or slowing has led to a urry of research in this eld. Anne Magurran reviews methods of evaluating temporal turnover in Chapter 7, but argues that there is still much to be learnt about baseline changes in ecological communities. A single index of biodiversity limits the amount of information that can be conveyed. An alternative is to examine the structure of a community in terms of its species abundance distribution or spatial patterning in more detail. This is the subject matter of the next section of the book. In Chapter 8 Anne Magurran and Peter Henderson explore the ecological context of commonness and rarity, and discuss methods that can be used to identify and track common and rare species. A species abundance

distribution is the formal description of the abundance of the recorded species in a community, as well as a tool that is widely used to compare communities and to test hypotheses about community structure (McGill et al. 2007). Brian McGill examines species abundance distributions in detail in Chapter 9. After summarizing current methods of studying species abundance distributions, he suggests a new way to visually display species abundance distributions that does not suffer from some of the limitations of earlier graphical methods. He also presents a detailed analysis of which quantitative measures behave well under small sample sizes and which measures are truly independent of each other. Based on this he offers some guidelines on which measures to use under several scenarios. One of the main challenges with regard to species abundance distributions is how best to t them. In Chapter 10 Sean Connolly and Maria Dornelas critically evaluate different approaches for tting species abundance models to data and examine methods of quantifying goodness of t. As they conclude, model selection statistics are a promising development and have advantages over traditional approaches such as graphical inspection and comparative analyses of goodness-of-t statistics. Whereas some ecologists focus on the distributions of species abundances others are concerned with the spatial placement of species. As Kevin Gaston and Fangliang He argue in Chapter 11, one of the most fundamental units of biodiversity is the presence or absence of a species in a given site, such as habitat patch, an island, or a grid square on a map. They show that simple species sites (r c) matrices, in which the presence/absence of different species (in rows r ) is given for a set of different sites (in columns c), lie at the heart of many biodiversity studies and are linked to patterns such as speciesarea relationships, nestedness, and gradients in diversity. Gaston and He explore occupancyarea relationships, occupancy abundance relationships, and speciesoccupancy distributions, and note that a key challenge is to estimate species abundance from occupancy. Brian McGill develops the spatial perspective in Chapter 12 by examining the implications of the spatial structure of biodiversity for management and conservation. New developments in spatial


statistics are explored and applied to questions such as is there variation in abundance across space? and are there interactions across space?. The analysis of spatial structure is an example of an area of biodiversity in which new analytical techniques are proving particularly important. Historically most investigators have used species (or in some cases morphospecies) as their biodiversity currency. However, some ecologists, for example Pielou (1975), were ahead of their time in recognizing that it is possible to increase the information content of biodiversity assessment by including taxonomic or phylogenetic information. This view has been reinforced by growing awareness of the need to conserve biodiversity function and by rapid advances in methodology. Recent developments in this eld are discussed in the next section of the book, on alternative measures of diversity. The section begins with a contribution by Evan Weiher on trait diversity. He argues in Chapter 13 that there are four conceptual aspects to trait diversity: the occupation of trait space, functional evenness, functional divergence, and the density of species packing. A rapidly growing set of indices is available and guidance is provided on the choices. As always the approach will depend on ones goal. For example, a multivariate method may be most appropriate if the goal is to assess the amount of trait diversity in a community. Phylogenetic diversity is another area in which large numbers of metrics are being developed. Much of the impetus behind this rapid expansion is the growing awareness that these measures have an important role to play in both conservation biology and community ecology. Mark Vellend, William Cornwell, Karen Magnuson-Ford, and Arne Mooers provide a conceptual overview of phylogenetic diversity in Chapter 14 and report the results of simulation analyses that examine articial communities constructed using a range of assumptions about phylogeny structure and assemblage composition. Vellend and coauthors also explore the qualitative and quantitative relationships among metrics and advise on choosing metrics for different purposes. They point out, for instance, that the sensitivity of phylogenetic diversity metrics depends to a large extent on the shape of the phylogenetic tree. Improved phylogenetic

information is, of course, underpinned by the revolution in molecular ecology. This means that rather than counting speciesor even evaluating traits and phylogeniesinvestigators can now directly evaluate the diversity of genes. Melanie Culver, Robert Fitak, and Hans-Werner Herrmann discuss these opportunities in Chapter 15. As they point out, genetic diversity can be measured using a variety of molecular genetic markers, each with a different evolutionary rate. Markers have different resolving power, so the choice of marker will depend on the biodiversity question, and the level of resolution needed to address that. As will already be clear, the methods presented in this book are relevant to a wide range of theoretical and applied questions. The nal section, on applications, presents a set of topics and case studies in which diversity measurement and assessment plays a fundamental role. Lise vres and Thomas Curtis argue in Chapter 16 that microbial diversity is the outermost frontier in the exploration of diversity. They note that the traditional species concept is useless in microbial ecology and focus instead on evolutionary relationships inferred from changes in molecules, primarily rRNA. vres and Curtis note the importance of sampling and look ahead to the advent of novel massive parallel sequencing as a means of providing a comprehensive examination of microbial communities. Although advances in microbial ecology are driven by technology, the assessment of microbial diversity is also dependent on statistical techniques, such as the non-parametric richness estimators devised by Anne Chao. Chapter 17 turns to another problem of considerable contemporary concern, that is disturbance and its impact on ecosystems. Maria Dornelas, Candan Soykan, and Karl Inne Ugland examine the use of biodiversity metrics to measure the effects of disturbance and observe that the sheer number of methods available can make it difcult to select an appropriate measure. This difculty is heightened by the lack of rigorous comparative studies exploring the merits of the different approaches. They argue that the most appropriate method will vary from case to case depending on the nature of the disturbance but recommend several options, including the use of multiple metrics. The empirical cumulative distribution function is


one new method that appears to have considerable merit. Traits-based metrics are also potentially valuable. Dornelas et al. conclude by emphasizing that more theoretical work is needed to understand the effects of disturbances on biodiversity metrics other than species richness. There are few landscapes in the world have not been modied by humans. Steven Chown and Melodie McGeoch ask, in Chapter 18, how the goals of biodiversity measurement are shaped by this transformation. Biodiversity assessments of modied landscapes such as agroecosystems draw on the techniques discussed in this book and, as elsewhere, the approach adopted in any particular case will depend on the question being posed. However, it may be informative to explicitly address management issues, for example when assessing the biodiversity of a landscape that is a tapestry of modied habitats such as hedgerows and monocultures, or contains elds under a variety of agricultural systems, for example conventional and organic farming. In another context, conservation managers often seek to reduce impacts and reverse transformation. Chown and McGeoch argue that r c matrices are a very useful addition to the toolkit of methods used to assess transformed landscapes as they make it possible to explore patterns across different levels of biodiversity, such as genes, traits, and species. Quantifying the loss of biodiversity is a task that increasingly preoccupies ecologists and conservation biologists. It is also a central goal in palaeontology and investigators who test ideas about extinction in the context of the fossil record use methods that are similar to those employed by conservation biologists. In Chapter 19 Peter Wagner and Kathleen Lyons review current palaeobiological methods for inferring extinction patterns. These extend from traditional methods that use information in stratigraphic ranges to approaches that exploit exact information about distributions of nds within stratigraphic ranges. As Wagner and Lyons show, the fossil record provides data that can be used to test a wide variety of extinction hypotheses. Michael Rosenzweig has been inuential in shaping views about species area and species time curves (Rosenzweig 1995). In Chapter 20 he is joined by John Donoghue, Yue Max Li, and Chi

Yuan in an examination of species density, particularly its use in assessing and comparing sites in a management or conservation context. The attraction of species density in such evaluations is clear. Although, as we have emphasized above, there is no single measure of biodiversity that serves all needs, many practitioners desire a few informative and intuitive metrics, ideally ones that appeal to politicians and policy makers. Species density is an obvious candidate but has a signicant drawback in that it does not scale linearly with area. Rosenzweig and colleagues develop estimates of species density that take the curvature of speciesarea curves into account and highlight its value as a useful indicator of environmental condition. Our conclusion, in Chapter 21, says that the measurement of biodiversity is growing (and will continue to grow) increasingly more sophisticated. This is to be welcomed as it allows for more nuanced discussions and more rened measures appropriate to specic questions. At the same time, the healthy growth of a tree requires regular pruning. Measurement of biodiversity is no different. Ecologists need to put as much energy into removing unsuccessful measures as we do into developing new measures. Finally, the increasingly complex ability of scientists to measure the multifaceted idea of biodiversity should not be allowed to distract from the societal and policy goals of conserving biodiversity. There is a real concept and relatively simple measures get us close enough to allow policy decisions and assessments to occur. This book covers a wide range of approaches and reects the activity and excitement at the frontiers of biodiversity measurement and assessment. We are conscious that there are aspects of biodiversity measurement that we have not dealt with or have mentioned only briey. These include issues such as population trends, the extent of habitats, the status of protected areas, the fate of threatened or invasive species, surrogate measures (for instance those based on remote sensing), and matters related to ecosystem services such as wild harvests. A single book could not do justice to all this material, and interested readers will nd that there is a growing literature that tackles it. However, we stress that the fundamental issues that underpin many of these alternative and broader measures


are addressed in the book. For example, a composite indicator or headline index is only as good as the estimates of species richness or species density subsumed within it, and sampling and detectablity issues need to be addressed in every study before robust conclusions can be drawn. As explained at the outset our emphasis in this book is on Darwins proportional numbers and kinds and we hope that it will prove a useful guide to measuring and assessing this beautiful diversity.

We are indebted to our contributors, to Bob May for writing the Foreword, and to Ian Sherman and

Helen Eaton for overseeing the publication of the book. In addition we are most grateful to Amy Deacon for drawing the hummingbird vignettes, and to Nichole Engelmann and Malissa Hubbard for compiling the index. We also thank the National Center for Ecological Analysis and Synthesis (NCEAS) for funding a workshop on species abundance distributions that allowed us to rst meet, to meet many of the contributors to this book, and to start many discussions on measuring biodiversity. Anne Magurran wishes to thank the University of St Andrews and the Royal Society of Edinburgh. Brian McGill thanks the University of Arizona, School of Natural Resources and the Environment, and his colleagues there.