14
Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability Author(s): John H. Lawton Source: Notes and Records of the Royal Society of London, Vol. 58, No. 3 (Sep., 2004), pp. 321- 333 Published by: The Royal Society Stable URL: http://www.jstor.org/stable/4142077 . Accessed: 10/06/2014 10:29 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. . The Royal Society is collaborating with JSTOR to digitize, preserve and extend access to Notes and Records of the Royal Society of London. http://www.jstor.org This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AM All use subject to JSTOR Terms and Conditions

Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

Embed Size (px)

Citation preview

Page 1: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

Japan Prize Commemorative Lecture: Biodiversity, Conservation and SustainabilityAuthor(s): John H. LawtonSource: Notes and Records of the Royal Society of London, Vol. 58, No. 3 (Sep., 2004), pp. 321-333Published by: The Royal SocietyStable URL: http://www.jstor.org/stable/4142077 .

Accessed: 10/06/2014 10:29

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

The Royal Society is collaborating with JSTOR to digitize, preserve and extend access to Notes and Records ofthe Royal Society of London.

http://www.jstor.org

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 2: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

Notes Rec. R. Soc. Lond. 58 (3), 321-333 (2004) doi 10.1098/rsnr.2004.0069

JAPAN PRIZE COMMEMORATIVE LECTURE:

BIODIVERSITY, CONSERVATION AND SUSTAINABILITY*

by

JOHN H. LAWTON CBE FRS

Natural Environment Research Council, Polaris House, Swindon SN2 1EU, UK, and Centre for Population Biology, Imperial College, Silwood Park, Ascot SL5 7PY UK

INTRODUCTION

Earth is the only planet in the entire universe where we know for certain that life exists. On this remarkable planet, approximately 1.7 million species of organisms have been described by biologists, but current work suggests that the true number of living species might be much higher than this-of the order of 10 million, possibly more. The key chal- lenges in biodiversity research are not only to catalogue life on Earth but also to under- stand how this diversity evolved, how it is maintained, and how we might hope to conserve it in the face of massive, and growing, human impacts. But before I tackle these major issues, I want to explain briefly how I came to select the scientific problems that have formed my life's work, and which led to this very great honour.

I am, first and foremost, an ecologist, and throughout my career I have focused my attention on that part of ecological science known as community ecology; that is, with patterns and processes that involve groups of coexisting species at one locality.

Community ecology is one of the underpinning components of biodiversity science, asking questions such as: How many kinds of species are there in a particular place, and why this number and not many more, or many fewer? How do these species interact, and with what consequences? And what happens to communities as habitats are fragmented? I will return to these and similar issues later.

Within this general framework, I have been privileged to investigate all kinds of inter- esting problems. I did my PhD on dragonflies. I have worked on predation by cats in an English village, termites and nematodes in Cameroon, and invading insects in blighted landscapes near London. I have explored problems as varied as biological pest control, the fractal dimension of vegetation, and organisms as ecosystem engineers. I have built mathematical models of nature, put her in bottles and controlled environment facilities, and manipulated populations and communities in the field. Wherever and whenever pos- sible I have watched birds. In the time available I can share very few of these activities

* This lecture was given on 21 April 2004, in Tokyo, Japan, on the occasion of the 20th Anniversary of the Japan Prize. John Lawton was awarded the 2004 Japan Prize for 'Observational, experimental and theoretical achievements for the scientific understanding and conservation of biodiversity'.

321 ? 2004 The Royal Society

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 3: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

322 John H. Lawton

with you. Instead my central theme starts with an apparently simple, not to say arcane, interest of mine-the insects that feed on a plant called bracken (Pteridium aquilinum), a common and widespread fern.

INSECTS ON BRACKEN AND SOME DIVERSIONS ALONG THE WAY

Bracken is extremely common throughout the British Isles, often growing in large patches covering hundreds of hectares, with no other species of plants present. The core of my work in community ecology started with the insects that feed on bracken at one

locality in northern England and gradually extended from there. The key point is that, at the outset, I never intended the bracken work to turn into a biodiversity study. That was a happy coincidence.

I first started thinking about working on the insect herbivores that feed on bracken in Oxford in the summer of 1970. Conceptually I was excited by a paradox that nobody else seemed to have noticed. At that time, a widely held view was that agricultural crops were

prone to outbreaks of insect pests because of their simplicity; crop monocultures lacked the complex checks and balances present in much more species-rich, natural communi- ties. However, bracken monocultures have all the uniformity and monotony of an arable

crop, yet hardly ever suffer major outbreaks of insect herbivores. I have never personally seen an outbreak on a natural bracken patch in Britain in over 30 years. Why?

More formally, in the early 1970s ecologists had become fascinated by the 'diversity- stability' problem, which asks the question: Are species-rich assemblages more stable than species-poor assemblages? Opinion was strongly divided, and the bracken system seemed to offer an opportunity to investigate the problem experimentally in the field. With hindsight it all looks a bit naive. We now know that there are several different mean-

ings of the word 'stability' in ecology, and at the time these were being confused by field- workers and mathematical modellers alike. I never did solve the diversity-stability problem, and still do not know why the populations of insects that feed on bracken rarely become sufficiently common to defoliate the plant! Instead, I ended up solving some dif- ferent problems.

The diversions

Almost everybody I talked to in those early days in Oxford, including the two leading fig- ures of the time in entomology (George Varley) and ecology (Charles Elton), expressed sur-

prise at my choice of plant. The consensus was that it lacked interesting herbivores, with

colleagues implying that it was for this reason an unusual plant. But how many species of insects might one expect to find on a plant like bracken? What would be normal?

We now know that 27 species of herbivorous insects regularly feed on the above-

ground parts of the plant in Britain and that at least five additional species attack the 'roots' (technically the rhizome). Add a few species that occasionally also feed on the plant, and at least 40 species of insect herbivores are known to exploit it. Is this fewer, or more, species than one might expect? How could I work out what to expect?

From Dick Southwood's pioneering work in the 1960s I knew that the size of the cur- rent (and possibly historical) geographic range of a plant species might be important in

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 4: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

Japan Prize Commemorative Lecture 323

determining its herbivore species load. I therefore set about compiling lists of the insect

species feeding on other widespread and common plant species, documented in the

Biologicalflora of Britain published in the Journal of Ecology between 1948 and 1973. The results showed that there was nothing unusual about the species richness of the insects feeding on bracken. The number was absolutely average for a common and wide-

spread British plant. Although I did not realize it at the time, this was my first foray into what we would

now call 'macroecology', using published data to study large-scale problems in ecology; in this case it was: How many species of insects feed on different kinds of plants over an entire country? However, the analysis was crude. Could it be done more thoroughly? Now the diversions came thick and fast, the first from Dieter Schr6der, who invited me to Switzerland to do a more thorough job of understanding the role of host-plant geo- graphic range in determining the number of herbivorous insect species exploiting British

plant species. Why geographic range? A few years earlier, the 'species-area relationship' had been

brought to the forefront of ecological science by Robert MacArthur and Edward Wilson in their seminal book The theory of island biogeography (1967). They showed that large islands hold more species than small islands, which is hardly surprising; the regularity of the relationship is (or was at the time) quite unexpected, as was their elegant and simple theoretical explanation for the pattern. Schr6der and I showed that exactly the same rela-

tionship held for insects on plants, with the size of a plant's geographic range substitut-

ing for island area. Biologically, the result is unsurprising, because the great majority of insects feed on only one, or a very few, species of plants. Their hosts are 'islands' sur- rounded by a 'sea' of inedible plant species. As a result, UK plants with large geograph- ical ranges are fed on by more kinds of insects than plants with restricted ranges, again in a very regular and predictable way. And the results confirmed that there was nothing unusual about the number of insect species exploiting bracken.

Why does size of geographic range have such a strong effect? Put simply, the number of species is determined by the rate at which they colonize and accumulate on a plant in

'ecological time', and the rate at which they evolve to exploit it in 'evolutionary time'. These processes of positive accumulation of species are opposed by the rate at which

species are lost from the system by local or regional extinctions. The balance of these

opposing processes determines species richness. Widespread plants are more likely to be found and colonized by herbivores, because widespread plants present bigger 'targets'; and insects exploiting plants with large ranges are less likely to be lost over time because

large populations are less likely to become extinct than small populations. Moreover, widespread plants 'sample' a wider range of environmental conditions than restricted-

range plants, allowing herbivores with different ecological requirements to colonize the

plant in different parts of its geographic range. Over and above the effects of geographic range, Schrider and I also showed that 'plant

architecture' had a major effect on insect species richness. Comparing plants with ranges of similar size, large, complex plants such as trees host more insects than small, simple plants such as grasses. Once again, the pattern was surprisingly regular. These results generalize to the now widely established rule in ecology that physically complex habitats

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 5: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

324 John H. Lawton

of all kinds generally are home to more species of organisms than simple habitats. I

began to realize that macroecology had much to offer, and that although the natural world

might look overwhelming at first sight, biodiversity conforms to some rather simple rules.

Shortly after I finished the work with Schr6der, Don Strong, who had been working independently on similar problems in Florida, contacted me and suggested that he, Dick Southwood and I get together. The eventual result was Insects on plants: community pat- terns and mechanisms, published in 1984, which brought together essentially all that was known at the time about the evolutionary and ecological determinants of the biodiversity of herbivorous insects. If this seems an obscure subject, remember that herbivorous insects dominate life on Earth. About a quarter of all the known species on our planet belong to this group of animals. If you understand how diversity in herbivorous insects is determined, you understand a great deal about the diversity of life in general.

In short, from the mid-1970s onwards, I became totally absorbed by plant-insect inter- actions, and as a result I had hardly any time to think about diversity and stability.

I did try to get back to my original objectives. As I began to properly understand the mathematical models being developed to address the diversity-stability problem, it became clear that one plausible reason why bracken-feeding insects rarely increase

markedly in abundance might have to do with the structure of the food-web in which they are embedded. Could we learn anything about stable and unstable food-web configura- tions by modelling the problem?

I discussed these ideas with Stuart Pimm, who had been an undergraduate student of mine in Oxford. What emerged was very different from what I had vaguely planned. We ended up exploring a variety of problems, starting with: What determines the length of food chains? Does the flow of energy to the top of the chain limit length, or are there

dynamic constraints driven by species interactions? We concluded, contrary to received wisdom at the time, that dynamic constraints were more important than energy flow. We then went on to tackle other issues about the topology of food-webs that were equally controversial.

Looking back 30 years, our models were crude, and the empirical data then available on food-webs woefully inadequate, not to say seriously misleading, but the work set in train a whole new subdiscipline of ecology, focusing on food-webs that continues to this

day. But it did not tell me anything about bracken!

By the late 1970s there was no going back to bracken as a study of diversity and

stability. Each of the diversions had become a major research agenda for me in its own

right. However, I did manage to keep the basic community ecology work running on bracken patches at a site known as Skipwith Common near York in the north of England (I moved to York in 1971). What did I learn?

BRACKEN-FEEDING INSECTS: FROM LOCAL TO GLOBAL PROCESSES

I sampled bracken-feeding insects on a patch of bracken growing in the open at Skipwith throughout spring and summer between 1972 and 1990, and conducted a similar but shorter study on bracken growing under trees. I also started a national survey, sampling

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 6: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

Japan Prize Commemorative Lecture 325

insects on bracken patches wherever and whenever I had the opportunity to do so as I travelled around the UK.

Local processes at Skipwith Common

Of the 40 species of insects that have been recorded feeding on bracken in Britain, a total of 24 were found on the above-ground parts of the plant at Skipwith. The average num- ber of species recorded on the open patch each year was 17.6, with a minimum of 15 and a maximum of 19. The woodland patch held slightly fewer species-from 13 to 16, with an average of 14.6.

As I expected, maximum densities of individual species were very low, with huge reserves of uneaten foliage. Frustratingly, however, despite all these years of observation and many experiments, I am unable to say in detail how any of the populations were reg- ulated. There is evidence that some were held in check by natural enemies (predators, parasites and diseases) and others, somewhat surprisingly, were limited by food supplies. Bracken, it turns out, is biochemically nasty, and only very small parts of the plant may be edible for some of the herbivores at any one time. But whatever the detailed mecha- nisms, the result in the short term is a high degree of predictability in the rank order of

species abundances, with the rare species staying rare and the common species staying common. However, this predictability decays slowly over time (rank abundances are more similar in two consecutive years than 20 years apart).

Finally bracken has extra-floral nectaries (nectaries outside flowers), first described for bracken by Francis Darwin in 1877. In the spring and early summer the young nec- taries actively secrete small quantities of a sticky, sugary liquid; when the bracken foliage matures, nectar production stops. The secretion is predominantly glucose and fructose, with small quantities of amino acids, and is extremely attractive to ants. Many other

species of plants also have extra-floral nectaries, and in general the relationship with ants seems to be symbiotic: the ants are attracted to, and feed from, the nectaries, and in return offer the plant protection from insect herbivores by attacking any they encounter on the

plant (the ants do this to obtain protein, not because they feel benevolent!). In bracken we seem to have moved on one step further in the arms race between ants

and herbivores. Several experiments were unable to demonstrate any effect of the ants on the abundances of bracken-feeding insects, which have evolved clever ways of avoiding the ants: for example, many live inside galls or rolled leaves; others 'bleed' highly dis- tasteful body fluids if attacked by an ant; others only exploit the plant once ant activity ceases later in the season and so on. The bracken-nectary-ant-herbivore story is a won- derful illustration of the richness of biological interactions that can be revealed by the

simplest of biodiversity studies.

Why do rank abundances change with time, and why does it matter?

As I have just mentioned, most common species of bracken-feeding insects at Skipwith stayed common and the rare species stayed rare throughout the study period, but this con- cordance (which can be precisely measured statistically) decayed over time, resulting in some species that were common early in the study becoming rare, and some initially rare species becoming commoner.

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 7: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

326 John H. Lawton

This simple observation (which we now know is true for most assemblages of species that have been studied for sufficient periods) is driven by the way in which environments themselves change over time, and is currently an active research area in ecology. Here we need simply note that it has important implications for conservation. It means that in the long run initially common species face decline and possibly eventual extinction. No

populations at one locality are safe forever. I shall return to this point in due course.

The species-area relationship again As I extended the bracken study throughout Britain, it soon became apparent that the size of a local bracken patch determined the number of species found in it-another

species-area relationship, although in this case rather a weak one, because species accu- mulated very slowly with increasing area. Hence what I am about to say about the large- scale biogeography of bracken-feeding insects is not seriously affected by this local

species-area relationship. We can effectively ignore it as a 'second-order' (although interesting) problem as we move to bigger issues.

These bigger issues centre on the determinants of bracken herbivore richness across entire biogeographic regions.

Sketching a bigger picture Two or three years after moving to York and setting up the Skipwith project, I went to the

library to look up something about bracken (I forget what), and stumbled on the fact that the plant grows naturally on every continent except Antarctica. Again, I could pretend that I chose it for this reason. I didn't. It was another accident.

I remember dashing home that night and saying to my wife, Dot, something like: "Do

you realize that bracken grows all over the world? At last, here's a system where nature has probably done the same experiment in community assembly independently several times on different continents. If there are rules, this is the way to find them!" Dot's reply was brilliant: "Oh good. Now you get to go bird watching all over the world, at some-

body else's expense." I did birdwatch, I must confess. But I also sampled bracken. To see where we are heading, consider one of the simplest questions one could ask

about a community. What determines the number of species it contains? The Skipwith open site had an average of just over 17 species each year. Why 17? In crude order-of-

magnitude terms, why not 2, or 170? This most basic of all aspects of community struc- ture turns out to have surprisingly little to do with local processes such as predation or

competition, the traditional concerns of community ecology. Before we look at the larger picture for bracken and other systems we need a concep-

tual framework. Assembling communities is a multi-stage, multi-layered process. It starts with a regional pool of species, exactly as MacArthur and Wilson recognized over 30

years ago. The pool, or metacommunity, exists within a biogeographic region, and local communities assemble themselves from this pool through a series of filters. The filters themselves work on different spatial and temporal scales and they overlap. Broadly, they are these. First, species have to arrive before they can establish populations. The proba- bility of this happening depends on where species occur--that is, on the structure of their geographic ranges and on the isolation of the site in question. If species can reach a site

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 8: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

Japan Prize Commemorative Lecture 327

they might still find the environment unsuitable; strong environmental filters work on all communities. More subtle processes operate at the landscape scale, processes that my colleague Bob Holt calls 'ecology at the mesoscale', including the size, shape, number and spatial arrangement of habitat patches, all of which can influence population persist- ence. Only at the lowest level do local species interactions such as predation and com-

petition have an impact on the survivors that made it through all the other big filters. Different species of insects have evolved to exploit bracken in different parts of the

world. Sometimes they are related to species exploiting the plant on another continent, but many are not. Hence, by repeating the kind of sampling I had done at Skipwith and

throughout the UK, on bracken in other parts of the world, I could start to test how local communities of bracken-feeding insects were assembled from different regional pools.

Variation in the size of the regional pool of insect species exploiting bracken in dif- ferent parts of the world turned out, once again, to be a simple function of how common and widespread bracken is in each geographic region. There is a strong geographical species-area effect. It is as simple as that. And at these large scales, the ecological processes of immigration and emigration cannot generate the relationship. Instead, as Mike Rosenzweig has argued, species-area relationships on geographic scales are fun-

damentally products of the rate of speciation, which is higher in bigger areas, and the rate of extinction, which is lower in bigger areas. In addition, substantial differences in habi- tat and climate across large geographic regions mean that different insect species occur in different portions of the total range of widely distributed plants, but not within the

ranges of more geographically restricted plants. This geographic species-area relationship for bracken-feeding insects is essentially

the same simple, but powerful, macroecological pattern that Dieter Schr6der and I observed for different species of plants and their insects within a single country, namely the British Isles. It differs in involving a single species of plant with variable range-sizes in different countries. But the underlying processes and outcomes are the same.

The final question is how this large-scale variation in regional richness maps onto the number of species coexisting locally on a particular patch of bracken. Again, and unex-

pectedly, the answer is very simple. Local richness is a 'proportional sample' of the

species in the regional pool. Local patches never hold all the species found regionally; rather, to a first and fairly crude approximation, in any one year a local assemblage of

bracken-feeding insects will hold about half the species in the regional pool, with minor variation in numbers driven by the size of the local bracken patch. But because regional pools vary strongly in size, so too does local species richness on similar-sized bracken

patches in different parts of the world. I found as few as three to five species in the moun- tains of New Mexico and on bracken growing in the Eastern Cape of South Africa, com-

pared with 14 in Papua New Guinea and 17 at Skipwith. Finally, and remarkably, we now

know that most (but not all) local assemblages of any kinds of organism (plants, birds, butterflies, fish) are simple, proportional samples of the species found regionally.

Vacant niches

A direct corollary of these results is that communities of bracken-feeding insects in dif- ferent parts of the world contain 'vacant niches'-a means of exploiting the plant in one

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 9: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

328 John H. Lawton

part of the world that is absent from another. Examples would be an insect that bores into the stem of the plant, or one that forms galls on the foliage, found in some countries but not in others. The notion of vacant niches was first suggested, as far as I am aware, by the great ecologist Evelyn Hutchinson in 1957, and it flies in the face of the widely held belief that 'nature abhors a vacuum'. Nor do there seem to be limits to the number of

species exploiting a particular occupied niche; sometimes it is one species and sometimes several. Many ecologists feel uncomfortable when confronted with both observations, believing that species evolve to use all available resources, and that there are hard limits to local richness. Neither is true in bracken, and I doubt that they are true for many other communities.

LOCAL ABUNDANCE AND SIZE OF GEOGRAPHIC RANGE

I want now to move briefly to another major macroecological pattern. Drawing on my national survey work, Kevin Gaston and I noticed that locally abundant species at

Skipwith, Chirosia and Dasineura flies for example, tended also to be geographically widespread throughout the UK. In contrast, species that were rare at Skipwith were found in fewer places. The sawfly Stromboceros delicatulus is a good example. The result is a

broad, statistically significant positive correlation between average local population abundances of species at Skipwith and the size of their geographic ranges.

We now know that this interspecific range-abundance relationship is one of the most robust and regular patterns in ecology, ranking alongside the species-area relationship in its importance and generality. The pattern appears at many scales from landscapes to con-

tinents, and although there are some exceptions, they are few. There are at least nine theoretical mechanisms that can generate positive relationships

between the local abundances and regional distributions of species. As with several other

patterns in macroecology (for example the species-area relationship) it is extremely unlikely that there is a single correct explanation, with the result that it will usually be more profitable to ask questions about the relative contributions of several processes rather than seeking a single mechanism. Such patterns may be robust over a wide range of scales because they can be generated by several processes. None of the theoretical mechanisms has unequivocal and universal support; most of them have some support, some of the time, and distinguishing between the mechanisms and sorting out their rela- tive contributions is far from easy. For present purposes it is sufficient to know that the

relationship exists. I want now to think about an important consequence that flows from

it, linking the interspecific pattern to the equivalent intraspecific pattern. Population abundances (as we have seen) and geographic ranges of all species natu-

rally wax and wane in response to changing environments. It follows logically that if the

range of a species expands, so too must its average abundance at those sites where it occurs, and vice versa. Empirically, individual species must be able to move up and down the interspecific range-abundance correlation, generating their own intraspecific rela- tionship. It is therefore satisfying to note that positive intraspecific range-abundance cor- relations are predicted by all the main theoretical mechanisms generating the interspecific correlation, at least under some if not all circumstances. Moreover, a grow-

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 10: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

Japan Prize Commemorative Lecture 329

ing body of empirical data, particularly for well-studied birds and butterflies, is consis- tent with the general expectation that intraspecific increases (or decreases) in geographic ranges and local abundances go hand in hand. Finally, many host-specialist plant-feeding insects, including those found on bracken, are rarer per plant on small isolated patches of hosts than on larger, more continuous patches.

With Andy Gonzalez and other colleagues, I have also tested the prediction using the small arthropods (mites, spring-tails, tiny spiders) that live in moss-covered rocks. When we fragmented these mossy miniature landscapes by scraping moss from large areas and

leaving small, undisturbed patches (the experimental equivalent of felling a forest and

leaving small stands of trees), many formerly scarce and local species became extinct in the remaining moss patches, and the survivors becoming generally rarer (occurring at lower densities within remaining patches) and less widespread (found in fewer patches), exactly as expected.

Notice that neither local abundance nor size of range can be treated as the independ- ent variable in these relationships. The theory shows that each can affect the other, or both are a consequence of a third variable such as resource availability. Forced reductions in geographic ranges, as in the little moss systems, lead to reductions in population den- sities in surviving patches. Equally, forced reductions in population density will lead to declines in a species' geographic range. The only caveat is that such linked changes may not happen instantaneously, so that in the short-term densities and ranges may even

respond in opposite directions (there are empirical examples of exactly this). But in the

longer term, ranges and population densities must expand or decline together.

LESSONS FOR THE CONSERVATION OF BIODIVERSITY

I have taken a long time to get to the conservation implications of these studies, but I now want to review at least some of them. Before I do I must stress that I am not the sole, or even the main, contributor to this body of conservation science. I am one among many to realize the implications of the species-area and range-abundance correlations for the conservation of biodiversity.

All over the world, human activities are destroying natural and semi-natural habitats at an alarming rate, fragmenting them and degrading them. Isolated patches of woodland in arable or urban landscapes are habitat fragments. Selectively logged forests are

degraded habitats, and in practice fragmentation and degradation often operate together. Andrew Balmford and colleagues recently estimated that human activities are currently fragmenting and severely degrading about 0.5-1.5% of what they refer to as 'wild

nature'(natural and semi-natural terrestrial and coastal habitats) every year. It may not sound much, but 0.5-1.5% a year amounts to about 15-30% in a human lifetime. Moreover, recall that we have historically already destroyed about 50% of wild nature for our farms, cities, factories, roads, reservoirs and so on; if we carry on as usual, within the lifetime of my grandchildren there will be precious little else left to destroy. It is more difficult to calculate comparable numbers for marine habitats, but we know that there is considerable destruction there also, in the world's shallow seas and coral reefs.

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 11: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

330 John H. Lawton

The consequences for biodiversity are inevitable. It is easy to understand why species are lost from degraded habitats, which may no longer contain suitable living conditions. It is less obvious, but nonetheless true, that fragmented habitats also lose species even if the surviving patches remain pristine. Fragmentation creates islands, and the

species-area and range-abundance relationships (and the mechanisms underlying them) say that species will inevitably be lost from surviving habitat patches, with more surviv-

ing in large patches than in small ones, because of the increased risk of extinction in

small, isolated populations. Add to this the simple fact that in the longer run, as with bracken insects, even initially common species may decline and become rare as environ- ments change, and it becomes easy to see why extinction for some species in small habi- tat patches is bound to happen. It may take time, but it will happen.

We can actually be more precise than this. Drawing together a very large number of

studies, on average the species-area relationship says that for every 90% reduction in habitat area (from 1000 to 100 hectares, or from 10 hectares to 1 hectare), about half the

species found in the larger patch will eventually disappear from the smaller, surviving fragment. And the losses are not random. For example, theory (including some of the food-web models alluded to earlier) and a growing body of empirical data suggest that

species feeding higher in the food-chain are more vulnerable to habitat fragmentation than species feeding lower in the food-chain. That is, food-webs tend to collapse from the

top down as patches decrease in size. Given that conservation biologists and the thinking public generally care more about saving tigers than termites, this is bad news.

The human response to these challenges is to create protected areas for wild nature, in the form of nature reserves, national parks, 'no-take' zones and so on. Clearly such pro- tected areas are important, and without them the situation would be even more dire than it already is. But, equally, protected areas are increasingly just islands in a sea of

destroyed, degraded or heavily modified habitats. The smaller each protected area is, the more difficult it is to maintain viable populations within them. That is why, in simple terms, they need to be as large as possible. The Convention on Biological Diversity requires all countries to designate 10% of their land area as protected (marine habitats do not currently enjoy even this target). The species-area relationship tells us that if most

species only survive in protected areas that amount to 10% of the land surface, roughly half of all terrestrial life on Earth is doomed to extinction. Of course, many species will survive outside reserves, but then the Convention does not require 10% of all habitats to be protected, and for some habitats, along with their uniquely dependent species, already less than 10% survives. I also doubt that the terrestrial target will be effectively imple- mented by many nations, out of greed, corruption, poverty or ignorance. This is why we now have a looming extinction crisis for life on Earth.

Climate change

Human destruction of habitats, unsustainable harvesting, and pollution will all continue to reduce populations, and fragment and reduce geographic ranges of species for the fore- seeable future. But there is now an even bigger emerging threat to biodiversity, namely climate change.

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 12: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

Japan Prize Commemorative Lecture 331

In my view, human-induced climate change is the biggest challenge facing the human race. It is already under way, and is getting worse; how much worse will depend on how much more fossil fuel (coal, oil and gas) we decide to consume and discharge as carbon dioxide into the atmosphere. I do not have time to say anything substantial about climate

change, except to touch briefly on its probable impacts on biodiversity. Climate change means that most of our protected areas will eventually turn out to be

in the wrong place; that is, as climatic zones shift, many of the plants and animals adapted to the conditions in a reserve when it was set up will no longer be able to survive there.

They will have to migrate to follow their preferred climatic conditions. But in an increas-

ingly fragmented world, migration across hostile, heavily modified habitats may be

impossible for many species. The alternative is extinction. For other species there may be nowhere to go, because the particular combinations of temperature, rainfall and sea-

sonality to which they are adapted may simply disappear from the face of the Earth.

Incidentally, the arguments do not simply apply to protected areas. They apply to all

habitats, inside and outside the world's network of protected areas. A recent analysis by Chris Thomas and colleagues published in Nature shows the scale of the problem. Taking the 'mid-range' climate warming predicted for 2050, they conclude that between 15% and 35% of all terrestrial species will be threatened with extinction, as their habitats shrink and shift. This is over and above the inevitable extinctions driven by the habitat

loss, over-harvesting and pollution just discussed.

THE SCALE OF THE HUMAN ENTERPRISE

Why should we care about extinction? More than 99% of all species that have ever lived are now extinct. Moreover, on at least five occasions in the last 600 million years, there have been mass extinctions that have eliminated a very large proportion of species living at that time. The 'big five' seem to have been driven by cataclysmic events, although experts argue about exactly what. The looming, contemporary extinction crisis is differ- ent. It is driven by just one species-us.

How big is (or will be) the sixth mass extinction? In 1995 Bob May, Nigel Stork and I did some crude but useful calculations. Using the fossil record, we worked out that a

very rough estimate for 'natural' or 'background' extinction rates is about one species a

year. During the nineteenth and twentieth centuries human activities started to accelerate extinctions, so that over the past hundred or so years, for well-studied and well-docu- mented groups such as birds and mammals, extinction rates rose to somewhere between 100 and 1000 times the background rate. Until very recently, there was considerable con-

troversy about whether extinction rates for other less well-known groups, insects for

instance, were comparable. We now know that they are, at least for butterflies, revealed

by an analysis that Jeremy Thomas, I and several other colleagues have just published in Science. Finally, as we look ahead, knowing projected rates of habitat destruction and the additional threats posed by climate change, it is difficult to avoid the pessimistic conclu- sion that extinction rates will continue to rise to at least four orders of magnitude (10 000 times) greater than the background rate. There is a sixth mass extinction, and it is

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 13: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

332 John H. Lawton

happening as we speak. Do not expect evolution of new species to fill the gap. It will hap- pen eventually, but not for millions of years.

There are all sorts of reasons to care about this catastrophic loss of species. They hinge on moral, ethical and aesthetic arguments, utility (many species are known to be useful or could be so), and the notion that species-rich ecosystems may deliver more reliable

'goods and services' such as clean water, healthy soils, and so on. But there is an addi-

tional, even more compelling argument. Coal miners in Britain used to take a canary into the mine to warn against the build up of dangerous gases. Canaries were more sensitive than people; when the canary died it was time for the miners to get out. Think of the

looming crisis of extinction as flocks of canaries in the mine of human activities. Extinctions on a massive scale warn us that the human enterprise is unsustainable in its

present form. We ignore the warning at our peril. It is easy to become bogged down in the special details of why any particular species

is threatened with extinction. I have tried to simplify the arguments by focusing on the

big picture, through the species-area and range-abundance relationships, and the nature of population variation. Yet there is an even simpler way to put it.

In a remarkable book, Stuart Pimm has brought together some measures of the scale of the human enterprise. Over the past decade there has been a series of specialist arti- cles in Nature, Science and other mainstream scientific journals that attempt to measure the impact of people on the planet. The articles are not easily accessible to a non-profes- sional audience. What Stuart does is take us through the key calculations and assump- tions in these papers, check the supporting data and logic, and summarize the conclusions. It makes stark reading. Human beings now take, for our own use, 40% of all terrestrial plant production every year, for food and fibre. We discard a great deal after

harvest, but we get first call. Nine-tenths of the world's oceans are a biological desert. In the remaining 10% we use between a third and a half of all production; as Daniel Pauly has put it, one in every two diatoms in the sea ends up in a fish caught by people. This is

why there is a global fisheries crisis. We also take 60% of all readily available fresh water

(what Stuart calls 'accessible run off'; there are huge quantities of fresh water in the polar ice-caps, but it is hardly readily available at any realistic economic cost). In other words, to a first approximation, every year our species now takes onto itself roughly half of all the useful stuff on the planet. The Garden of Eden is half the size it used to be. Is it any wonder that we have a crisis of extinction?

Now consider what this says about the sustainability of the human enterprise. Human activities (such as population numbers and economic growth) have a doubling time of

anywhere between 20 and 50 years. Manifestly, using existing technologies and 'business as usual' we cannot double the human enterprise again on a finite planet. We ignore the canaries of biodiversity at our peril.

It is not hopeless. There are many, many things we can do, new technologies to adopt, new ways of living within our means. But we must act now, and act quickly. It all seems a very long way from a small patch of bracken in the north of England, and indeed it is. But to do ecological science is to shine a spotlight on a wonderful world, to explore the beauty and mysteries of the only planet in the universe where we know for certain that

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions

Page 14: Japan Prize Commemorative Lecture: Biodiversity, Conservation and Sustainability

Japan Prize Commemorative Lecture 333

life exists. Surely it is not beyond the wit and wisdom of humanity to hand on that planet to our grandchildren in at least as good a shape as that which we ourselves inherited?

SUGGESTED FURTHER READING

I never intended this to be a lecture for specialists. Rather, I have tried to make my sci- ence accessible to as wide an audience as possible. Accordingly, I have deliberately not

provided an exhaustive (and for many, exhausting!) list of references to support all the scientific statements I have made in this essay. Readers interested in finding out more are

encouraged to consult the following books.

Blackburn, T. M. & Gaston, K. J. (eds) 2003 Macroecology.: concepts and consequences (43rd Symposium of the British Ecological Society). Oxford: Blackwell Publishing.

Daily, G. (ed.) 1997 Nature's services. Societal dependence on natural ecosystems. Washington, DC: Island Press.

Gaston, K. J. & Blackburn, T. M. 2000 Pattern and process in macroecology. Oxford: Blackwell Science.

Lawton, J. H. 2000 Community ecology in a changing world (Excellence in ecology, vol. 11) (ed. O. Kinne). Oldendorf/Luhe: Ecology Institute.

Lawton, J. H. & May, R. M. (eds) 1995 Extinction rates. Oxford University Press. Pimm, S. L. 2001 The world according to Pimm. A scientist audits the Earth. New York: McGraw-Hill. Strong, D. R., Lawton, J. H. & Southwood, T. R. E. 1984 Insects on plants. Community patterns and

mechanisms. Oxford: Blackwell Scientific Publications.

This content downloaded from 188.72.96.104 on Tue, 10 Jun 2014 10:29:47 AMAll use subject to JSTOR Terms and Conditions