Indicator Species

Indicator Species John H Lawton, Imperial College, London, UK Kevin J Gaston, University of Exeter, Exeter, UK, and University of Sheffield, Sheffield, UK r 2001 Elsevier Inc. All rights reserved. This article is reproduced from the previous edition, volume 3, pp 437–450, r 2001, Elsevier Inc.

Glossary Acid deposition Anthropogenic acidification of terrestrial and freshwater ecosystems by (primarily) sulfuric acid, derived from sulfur dioxide produced by burning oil and coal and deposited in rain and snow (acid rain), directly as particles (dry deposition) and as cloud droplets. All taxa biodiversity inventory (ATBI) The idea, first suggested by D. H. Janzen, that it might be feasible to produce a complete species list for all the organisms living in one place, a hectare of tropical forest, for example. The goal has so far proved elusive. Bioassay The use of living cells or organisms to make quantitative or qualitative measurements of the amounts or activity of substances. Community An assemblage of species populations that occur together in space and time. Ecotoxicology The use of test organisms (e.g., the water flea, Daphnia) to study the toxicity, pathways of accumulation, and breakdown of chemicals, particularly those manufactured by humans (e.g., pesticides).

Species as Indicators of the State of the Environment There are three distinct uses of the term ‘‘indicator species’’ in research in ecology and biodiversity. They are a species, or group of species, that do the following: 1. Reflect the biotic or abiotic state of an environment. 2. Reveal evidence for, or the impacts of, environmental change. 3. Indicate the diversity of other species, taxa, or entire communities within an area. This article explains, provides examples of, and evaluates each of these uses of the term, focusing primarily on terrestrial and freshwater ecosystems; broadly similar conclusions apply to marine ecosystems, but marine examples lie beyond the scope of the article. We pay most attention to the third use of the term ‘‘indicator species,’’ because this seems most appropriate for an encyclopedia devoted to biodiversity. The most up-to-date evaluation and review of indicator species in the scientific literature is by McGeoch (1998). She concentrates on terrestrial insects as ‘‘bioindicators’’ (in all three senses of the word) but the general principles that she discusses extend to all ecosystems and organisms, not just to terrestrial insects. Everybody knows that living organisms are sensitive to the state of their environment. Pollution from human activities kills many species and reduces the abundance of others. These

Encyclopedia of Biodiversity, Volume 4

Endemic species Species confined in their distribution to a particular geographic region. The size of the region is arbitrary (a species can be endemic to North America or to a tiny island). Hot spots A word with several distinct meanings. Here it is used to denote sites unusually rich in a particular group of species (e.g., birds), compared with average sites in the same geographic region. (The converse is a ‘‘cold spot.’’) Has also been used to denote centers of endemism (see Endemic Species), which need not be unusually species rich; it is not used in this context here. Paleoclimatology The study of past climates from fossils and other traces left in the geological record. Reserve selection algorithms Mathematical techniques used to maximize efficiency in the selection of protected areas for conservation. The efficiency criteria vary with circumstances but may, for example, be the minimum number of reserves with every species represented, or minimum cost.

changes in abundance can be used to assay the state of the environment.

An Example: Acid Deposition Sulfur dioxide, produced by burning fossil fuel, particularly coal, enters the atmosphere and is eventually deposited on terrestrial and freshwater ecosystems via three routes: (a) as tiny solid particles, (b) washed from the air in rain or snow, or (c) as droplets formed in clouds. Deposition often occurs hundreds of kilometers from the source. Dissolved in water, sulfur dioxide forms sulfuric acid, resulting in what is frequently referred to as ‘‘acid rain,’’ but because there are three principal routes involved in its transfer to terrestrial and freshwater ecosystems, it is more correctly called ‘‘acid deposition’’ (Erisman and Draaijers, 1995). Sulfur dioxide is not the only source of acidification; oxides of nitrogen, again produced by burning fossil fuel, are also involved, but sulfur dioxide is the main agent of acidification in most ecosystems. In terrestrial ecosystems, this deposition kills lichens and acidifies the soil, leading to changes in the vegetation. Lakes become progressively more acidic as deposition loads increase, until eventually they may become virtually lifeless. A trained biologist, visiting for the first time an area subject to acid deposition, will often be able to deduce that the habitat is being polluted simply by looking at the species that are present and those that ought to be there but are not. Beautifully

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clear Scandinavian lakes, lacking any fish or amphibians, supporting few birds and a species-poor and taxonomically unusual invertebrate fauna, have been reduced to this impoverished state by the transnational export of sulfur dioxide from coal-burning power-stations in the United Kingdom and elsewhere in Europe. Here, living organisms act as powerful indicators of the state of the environment and the damage being done to it by human activities, often performed many hundreds of kilometers away.

Management of European Rivers Because the species composition and richness of biological communities change as the environment changes, we can use species as indicators of the state of the environment for practical management purposes. The techniques have been particularly well developed to assess organic and inorganic pollution in European rivers, managed for recreation, fisheries, and drinking water. The advantages of using living organisms as indicators of water quality are that they avoid the need for expensive chemical analyses, and, probably more important, organisms integrate the impacts of pollutants over space and time. All chemical traces of a major pollution incident may disappear from a river in a matter of hours as the pollution is flushed from the system. Nonetheless, the biotic community may show evidence of the damage for many months. It is extremely difficult, and prohibitively expensive, for chemists to measure all the organic and inorganic chemical pollutants entering a river, and it is certainly impossible for them to work out what all the combined impacts of such a cocktail might be. But living communities reflect the integrated effects of all the compounds that find their way deliberately and accidentally into watercourses, and hence they act as sensitive indicators of the state of the environment. A valuable source of further information on the use of living organisms to monitor the environmental health of rivers and lakes is provided by Rosenberg and Resh (1993). Two widely used European examples of this approach are the German Saprobic Index, and RIVPACS in the United Kingdom. RIVPACS is now used by the Environment Agency to manage UK rivers. Both the German and UK approaches require accurately identified samples to be taken of the organisms found along sections of the river. RIVPACS focuses on invertebrates, the German index on invertebrates, microbes, and higher plants. Both rely on the fact that some species are extremely tolerant of pollution (the aquatic larvae of some chironomid midges, for instance), while others are extremely sensitive, particularly to the low oxygen levels produced by organic pollution (for instance, the larvae of many mayflies). The species present in the samples are given scores, depending on their known tolerances, and the data from all species are combined to produce a composite and very sensitive index of pollution levels for any particular section of a river.

Widespread Application Use of organisms to indicate the state of the environment is widespread, taxonomically and geographically, for a wide range of environmental issues. Use of species as indicators of

the state of the environment is not confined to freshwater, or to Europe and North America. A wide variety of organisms has been suggested, or used, as indicators of human impacts. In Europe, suites of plant, fungal, and insect species are only found in, and hence are good indicators of, ancient woodland; they are entirely absent from plantations, even though these may be several hundred years old. The use of lichens as sensitive indicators of air pollution is well known, but organisms as different as mites and geckos (agile, climbing lizards) have been used, or suggested, for similar purposes. Lichens have also been used as indicators of fire history in Brazilian cerado (a type of dry, scrubby forest), tiger beetles as indicators of tropical forest degradation in Venezuela, and day-flying Lepidoptera (butterflies and moths) as indicators of the state of seminatural grasslands for conservation in Europe. Many other similar examples exist.

Interpretation Requires Care In these and similar cases, considerable care is needed before a species or group of species can be used as reliable indicators of damaging (or beneficial) human impacts on ecosystems. All populations of living organisms fluctuate over time and vary in abundance spatially, because of natural variations in the weather, normal changes in the physical environment, and fluctuations in the abundances of natural enemies, competitors, and essential resources (food and shelter). Just because one or more species is declining does not mean that human impacts are to blame. In the case of lichens and atmospheric pollution or freshwater invertebrates and river quality, the links between anthropogenic pollutants and changes in the distributions and abundances of organisms are thoroughly researched and well understood. But even quite major declines in some species have proved exceptionally difficult to link to damage to the environment caused by people.

Amphibian Decline The so-called amphibian decline is a particularly dramatic example (Blaustein and Wake, 1995). In many parts of the world, population biologists interested in amphibians (frogs, toads, newts, salamanders, etc.) have recently become alarmed by apparent major declines in the abundance, and the complete disappearance, of many species from areas where formerly they were common, often in regions apparently remote from human impacts. The declines are not happening everywhere, and the magnitude of many of those that have been claimed is difficult to assess because of the lack of long-term data prior to the supposed population collapses; some of them may be perfectly natural. The worrying aspects of the phenomenon are that while it is apparently global in scope, the causal mechanism (or mechanisms) remains obscure. It has been suggested, for example, that the amphibian decline is indicative of rising global levels of damaging ultraviolet light (UV-B) caused by loss of the earth’s protective stratospheric ozone layer. Amphibian eggs, exposed in shallow water, and the adults with their thin wet skins may be particularly sensitive to UV-B, as are human sunbathers without sunblock.

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Others doubt the explanation. More recently a global pandemic has been implicated. But what should suddenly trigger lethal outbreaks of disease in amphibians is unclear.

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have at least two sets of data on the particular indicator species in question, taken in the same way, at the same place(s), on two separate occasions. More frequent sampling allows greater confidence in the direction of apparent trends and the detection of more subtle environmental changes.

Environmental Toxicology In all the examples so far, the organisms being used as actual or possible indicators of environmental health have been in their natural environment. There is another related but quite separate way in which biologists use the sensitivity of organisms to set environmental standards, namely in the science of environmental toxicology, or ecotoxicology for short. In many areas of human endeavor, the aim is to apply some beneficial technology with minimum environmental damage. Crop spraying with pesticides is a good example, and so is the discharge of treated effluent from a factory. Some environmentalists claim that these types of operations should not lead to any environmental contamination; factories should have zero discharges, and if we must use pesticides, they should be targeted to reach only the crop and the pest and not, for example, the soil, nontarget organisms, or adjacent watercourses. However, zero discharges or precision pesticides, if they can be achieved at all, can often only be obtained at great economic cost. The more pragmatic solution is to ask whether there are minimal levels of discharge, spray drift into watercourses, and so forth that cause no detectable environmental damage. To provide answers to this admittedly difficult question, environmental toxicologists use a wide variety of laboratory bioassays with standard organisms. Examples from freshwater include the alga, Chlorella vulgaris, the water flea, Daphnia magna, the amphipod shrimp, Gammarus pulex, and the rainbow trout, Salmo gairdneri. The fundamental problem is to try and establish acceptable levels of contamination. Defining ‘‘acceptable’’ obviously requires political as well as biological judgment. However, traces of a compound in water, air, or soil that cause no detectable changes in the performance (growth, survival, or reproduction) of the test organisms are clearly more acceptable than doses that kill 50% of the population (so called LD50 levels). Basically, the bioassays seek to set environmental standards for levels of potential pollutants in soil, air, and freshwater, using a range of standard laboratory organisms as indicators (Shaw and Chadwick, 1998), but there can be no absolute standards about what is safe or acceptable. The general trend in modern societies is for standards to gradually tighten.

Species as Indicators of Environmental Change If the amphibian decline (discussed in the previous section) is real, it is an example of a group of organisms acting as indicators not only of the state of the environment, but also as indicators of ongoing changes to the global environment, albeit of an unknown nature. In other words, given that species are sensitive to the condition of their environment, monitoring organisms not only tells you about the current state of an environment, but repeated monitoring can tell you about changes in that environment. To act as indicators of change rather than current environmental health, it is necessary to

Not all Monitoring is about Environmental Degradation Not all monitoring of species seeks to record environmental degradation. Increasingly after mining operations, for example, mine operators are required to restore spoil heaps and mine pits by sowing or planting native vegetation. Monitoring selected groups of common animals on nearby undisturbed control sites and on the restored land can give a good indication of the recovery of the entire ecosystem and of the success of the restoration project. For instance, when biologists monitored ant assemblages on abandoned, replanted bauxite mines in Australia, they found that the ants provided a good indication of the recovery of these ecosystems. Even after 14 years there were still differences between the ant communities found in the natural Eucalyptus forest and the restored land.

Historical Records of Change Lake Acidification It may not always be necessary to sample in real time. When anthropogenic acidification of lakes was first discovered, many people doubted that the phenomenon was real. In particular, there was considerable opposition to the notion from the power-generating industry, because solving the problem (by burning low-sulfur coal, adding ‘‘scrubbers’’ to power station chimneys to remove sulfur dioxide, or switching to natural gas) was inevitably going to be expensive. After all, there were few historic data on the state of the acidified lakes. Perhaps they had always been that way? Resolving the problem required knowledge of the fact that lake phytoplankton (the tiny, unicellular plants that float in the upper layers of lakes) are extremely sensitive environmental indicators, because different species grow best in very different conditions determined by nutrient status and pH (acidity). When algae die, they sink to the bottom where their bodies and characteristic pigments are buried and some are preserved (incipient fossils), particularly the resistant, silicious outer cases of a group called diatoms. An undisturbed core through the sediments records the history of a lake’s phytoplankton, with the oldest flora at the bottom. Cores showed unequivocally that many Scandinavian lakes that are acid now were not acid before the Industrial Revolution; the oldest diatomsFspecies not found in acid lakesFare gradually replaced in the sample column by acid-tolerant species. Diatoms are wonderfully sensitive indicators of environmental change (Figure 1).

Plants and Carbon Dioxide Herbarium specimens (pressed plants collected for taxonomic purposes) and fossil leaves can also be used as indicators of past environmental change. Another consequence of the rapid rise in the burning of fossil fuel since the Industrial Revolution has been an accelerating rise in the concentration

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Figure 1 The pH history of Lilla O¨resjo¨n, a 0.6 km2 lake in southwest Sweden. A core of the bottom sediments 3.5 m long records the history of the lake extending back to 12600 BP, using the valves (‘‘shells’’) of diatoms preserved in the deposits. Different species of diatoms have different pH preferences and can be classified accordingly. Acidobiontic species thrive in acid waters; alkilophilous species prefer more alkaline conditions. Combining data from the remains of all species of diatoms allows the pH history of the lake to be reconstructed. The lake has passed through four pH periods. A, an alkaline period after deglaciation. B, a naturally more acidic period. C, a period with higher pH, which started at the same time as agricultural expansion in the region, and D, a rapid, recent period of acidification. The post-1960 phase has no similarity with any of the previous periods. Reproduced from Renberg I (1990) Phil Trans. R. Soc. London B 327: 357–361, with permission from Royal Society of Publishing.

of atmospheric carbon dioxide, one of the main agents of ‘‘global warming.’’ We will deal with species as indicators of anthropogenic global climate change (as it is more accurately known) later. Here we want to focus on physiological and developmental responses within single species to rising carbon dioxide. If plants are grown in a greenhouse under different atmospheric carbon dioxide concentrations, from below the pre–Industrial Revolution levels of about 280 parts per million by volume (ppm), through what are roughly present levels of 350 ppm, to levels that may be reached by the end of the 21st century (700 ppm), several interesting things happen. In particular, in the present context, stomatal densities on the undersides of the leaves decline. Stomata are the tiny pores in the leaf surface through which plants take up carbon dioxide (needed for photosynthesis), and through which they lose water vapor. It has been known for a long time that plants control the opening and closing of stomata to optimize carbon dioxide uptake and reduce water loss. More surprising, we now also know that plants grown in high carbon dioxide have lower densities of stomata; something happens during leaf development to reduce the number of stomata. How and what is currently unclear. Why is simple enough. In a high carbon dioxide world, the plant needs fewer stomata to take up the carbon dioxide it requires and hence can satisfy the needs of photosynthesis and reduce water loss by developing fewer pores in the leaves. Now back to those herbarium specimens and fossil leaves. If you look at 200-year-old (and very precious) herbarium and modern specimens of the same species, sure enough, stomatal densities decline as global atmospheric carbon dioxide levels increase (Figure 2A). The same approach has recently been used to try and trace atmospheric carbon dioxide levels

throughout most of the Phanerozoic, from the time when plants first colonized the land. Here the method is more contentious, because different species of truly fossil plants with presumed similar growth forms have to be used in different geological periods. Nevertheless, the pattern of apparent changes in global atmospheric carbon dioxide concentrations over hundreds of millions of years, revealed by this method (Figure 2B and C), are in reasonable agreement with alternative, independent, and also contentious geochemical methods. Here is a really unusual use of species as indicators of environmental change.

Species as Indicators of Climate Change The Sensitivity of Species to Climate: Fossils Again Current, rapidly rising concentrations of atmospheric carbon dioxide are the primary cause of anthropogenic global climate change. However, the earth’s climate has always changed, naturally, with no intervention from human beings. One of the ways we know this is through the careful documentation of the types and distributions of organisms in the fossil and subfossil record. The science of paleoclimatology, which seeks to reconstruct the history of earth’s climate, relies heavily on changes in fossil and subfossil species assemblages to deduce what the earth’s climate was like thousands or even millions of years ago. To take one example, in the modern world many types of corals occur exclusively in tropical marine environments; it is a winning bet that fossil corals of the same type indicate an ancient tropical sea, even though the rocks bearing the fossils may now lie in much colder parts of the world. In more recent geological time, we can use changes in the distributions and abundances of plants and animals to trace

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Figure 2 Changes in stomatal densities of leaves as indicators of changes in atmospheric carbon dioxide concentrations. (A) Percentage changes in stomatal densities on the lower surfaces of the leaves from eight species of trees and shrubs collected from the English midlands and preserved as herbarium specimens. The oldest specimen was collected in 1750. As atmospheric CO2 has risen during and since the industrial revolution, so stomatal densities have fallen. (B, C) Assuming that similar effects occur in all species of plants, fossil leaves can be used as indicators of atmospheric CO2 concentrations extending back many millions of years. The CO2 content of the earth’s atmosphere appears to have fluctuated markedly and apparently naturally during the past 400 million years. Reproduced from Beerling DJ and Woodward FI (1997) Bot. J. Linn. Soc. 124: 137–153, with permission from Wiley.

major changes in the earth’s climate during the Holocene (the most recent geological past) and Pleistocene glacials and interglacials. Plant remains preserved in packrat middens in dry air of the southeastern United States attest a much wetter climate only a few thousand years ago. Hippopotamus bones and teeth dug up from under Trafalgar Square provide unequivocal evidence of a much warmer London. Pollen grains preserved in peats and lake sediments record in exquisite detail the march northward of European and North American forests from the end of the last glaciation 12,000 years ago (Huntley and Birks, 1983). The forests spread with remarkable speed (an average of about 200 m per year, but sometimes as fast as 2 km a year) to achieve present distributions in the northern parts of both continents from glacial refugia thousands of kilometres to the south (Figure 3A and B). The information is not won easily. It requires huge patience and great skill to identify thousands upon thousands of pollen grains extracted onto microscope slides. But once done, the record reads like a speeded-up movie, as spruce, oaks, white

pine, hemlock, beech, and chestnut swept north in successive waves through what is now the United States and Canada; in the more species-poor forests of Europe, pines were followed by birch, then oak. These invasions are as dramatic as any in human history, but they were silent and recorded only by pollen grains.

Contemporary Changes in Species Distributions Historical changes aside, there is now no doubt that the world is currently warming quite rapidly. An upward trend in global annual mean surface temperatures is apparent from about 1920, particularly over the last two decades (from c. 1980); global mean surface temperatures in July 1998 were the highest ever recorded. Do organisms act as indicators of these changes, perhaps, as with the freshwater species discussed earlier, acting subtly to integrate several of the changes humans find difficult to comprehend in the bald statistics? Climate change does not simply involve warming; it involves changes in rainfall, extreme weather events (droughts and

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Figure 3 The migration of trees across North America and Europe after the end of the last glaciation, revealed by pollen remains in lake sediments and peat. (A) The spread of oaks in North America, with radiocarbon ages in thousands of years (contours) and the present range of the genus (shaded). (B) Estimates of the overall rates of spread of trees on two continents, based on data of the type shown in part A. Reproduced from Williamson M (1996) Biological Invasions. London: Chapman & Hall.

storms), and even locally cooler conditions. All these complex changes should show up in changes in the distributions and abundances of organisms. They do. Species are proving to be extremely sensitive indicators of contemporary climate change, where historical records allow decent reconstruction of former and current distributions. Populations of Edith’s checkerspot butterfly Euphydryas editha are disappearing from southern California and northern Mexico, at the current southern end of its distribution, and from more lowland sites; sites where previously recorded populations still exist are on average 21 further north than sites where populations went extinct (Figure 4). These are exactly the changes we would expect in a warming world. Twenty years ago in northwest Europe, little egrets Egretta garzetta (small white herons) used to be rare visitors from the Mediterranean. Now they are breeding in northern France and southern England in an astonishing expansion of range. Populations of many other European birds, butterflies, and other organisms are spreading north at the present time, as the climate warms. Of course, none of this tells us whether the climate change that is certainly happening is ‘‘natural’’Fit could have happened anyway and may have nothing to do with anthropogenically produced greenhouse gassesFor whether it is indeed due to human activities. Using species as indicators of climate change tells us unequivocally that the earth’s climate is changing, but so does the mercury in the thermometer. What

neither tells us is why, and no end of work on species as indicators will solve that dilemma. As we have already seen, this situation is not unique to climate change. It generally holds whenever we use species as indicators of the state of the environment. Indicator species can tell us whether an environment is, or is not, changing. They do not tell us why the changes are taking place. That almost always requires additional detective work, although knowledge of an organism’s biology will frequently provide valuable clues. Three examples, using birds as indicators, illustrate the problem in more detail.

Birds as Indicators of Large-Scale Environmental Changes Birds are widely used indicators, because in Europe, North America, and other parts of the world where there are large armies of amateur bird watchers their populations and distributions have been recorded well enough, for long enough, to reveal major environmental trends.

Peregrine Falcons and DDT The catastrophic collapse of peregrine falcon Falco peregrinus populations throughout the northern hemisphere in the 1950s signaled widespread contamination of the environment by chlorinated hydrocarbon insecticides, first DDT, then other compounds such as aldrin and dieldrin. The total, and rapid, disappearance of these dramatic birds signaled to

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pesticides up the food chain, resulting in eggshell thinning, reproductive failure, and (in extreme cases) direct poisoning of adult birds. Although some populations have now recovered, signaling a recovery in environmental quality, the species is still missing from many parts of its former rangeFsome coastal populations in England, for instance. Nobody knows why.

Migratory Songbird Declines in North America In North America, considerable concern is currently being expressed over widespread declines in summer migrant birds, particularly warblers. Unlike the so-called amphibian decline, nobody questions the phenomenon; just like the amphibian decline, nobody really knows why it is happening. There is no doubting the data; many species are indeed declining very quickly, in as clear an indication as one wants that something is wrong with the environment, but what? Several possibilities exist, and they are unlikely to be mutually exclusive. One explanation focuses on the destruction of tropical forests in the birds’ wintering areas. Another suggestion is that there are other unknown problems there or on the migration routes. A third possibility is extensive habitat fragmentation and urbanization in the breeding forests of the eastern seaboard. This human modification of the northeast forests markedly increases nest losses of migrant songbirds to jays, crows, cowbirds, and racoons, all species that thrive in the slipstream of urban humans.

Declines in Formerly Common Farmland Birds in Northwest Europe

Figure 4 The fate of 151 previously recorded populations of Edith’s checkerspot butterfly, Euphydryas editha, in western North America. The populations ranged from northern Mexico to southern Canada and were visited by Camille Parmisan and other biologists between 1992 and 1996. Populations that had disappeared because of habitat degradation (e.g., loss of usable host plants) were omitted from the analysis. Dividing the populations into five, evenly spaced latitudinal bands between 301 N and 531 N (A) reveals that significantly more southern populations have gone extinct than northern populations; sites where previously recorded populations still exist were, on average, 21 further north than sites where populations were extinct. Extinctions were also higher at lower altitudes (B) (n is the number of populations in each latitudinal or altitudinal band). Both results are consistent with the effects of global climate warming on the butterfly, leading to a northward and upward shift in its geographical range. Reproduced with the permission of McMillan Journals Ltd, from Nature 282 (1996), page 766.

ornithologists that something was seriously wrong with the environment, but what? It took a great deal of clever biological detective work (see Ratcliffe, 1980) to link the decline of peregrine populations to the accumulation of these persistent

In the intensively agricultural areas of northwest EuropeF over the whole of lowland England, for exampleFa whole raft of formerly ‘‘common farmland birds’’ are also in steep decline (Tucker and Heath, 1994). They include skylarks (Alauda arvensis), European tree sparrows (Passer montanus), corn buntings (Milaria calaudra), gray partridges (Perdix perdix), and song thrushes (Turdus philomelos). Here the problem is now reasonably well understood, though many details remain unresolved. Modern farming is so efficient and clean that there is little for the birds to eat. Weeds are killed with herbicides, which remove both seeds and rich sources of insects that feed on the weeds. The crop itself is sprayed to remove insects and is harvested so efficiently that few seeds are spilled on the way. Modern farms are biodiversity deserts, an indication of the power of people to squeeze nature to the margins while apparently maintaining a green and pleasant land. If present trends continue, skylarks will be rare birds in Britain in 20 years.

Species as Indicators of Biodiversity The Nature of the Problem Common sense suggests that the known losses of plants and birds from European farmland will go hand-in-hand with much more poorly documented declines in many other, less familiar and cryptic taxa, from land snails to glowworms, and hoverflies to harvest spiders. In other words, changes in the distribution and abundance of well-known groups should

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serve as broad indicators of the status of, and changes in, a much wider sample of a region’s flora and fauna. The assumption here is that birds (or other conspicuous species) might serve as biodiversity indicatorsFthat is, as surrogates of overall biodiversity. But although it seems intuitively reasonable to use familiar, well-studied, and easily censused groups as indicators of what is happening to many other taxa, despite a great deal of research, the idea is actually contentious. Following (but slightly modifying) the work of McGeoch (1998), we can define a biodiversity indicator as a group of taxa (e.g., genus, tribe, family, or order, or a selected group of species from a range of higher taxa) whose diversity (e.g., overall species richness, number of rare species, levels of endemism) reflects that of other higher taxa in a habitat, group of habitats, or geographic region. The idea is simple enough, and if it can be shown to work, it is important because biologists then have a relatively simple means of assessing overall biodiversity for purely scientific reasons, for setting conservation priorities, or for monitoring the effectiveness of conservation management.

Taxa that have been Suggested as Indicators of Biodiversity The groups of organisms whose richness has been evaluated most thoroughly in the greatest number of places on earth are also the most familiar. The natural history sections of bookshops are dominated (sometimes exclusively) by volumes on plants and birds. If insects figure at all, butterflies will be on the top of the list, although there are fascinating differences between nations. Japan loves dragonflies. Birds, higher plants, butterflies, and dragonflies are all groups that occur in most places in the world but whose individual species are seldom so widespread. In much of the world they are also groups whose species are, relatively speaking, taxonomically well known and stable, readily identifiable, and have biologies that are well understood. They are easy to find, inventory, and count, and they are reasonably, but not overwhelmingly, diverse in any one place. These are all desirable attributes of groups that might be used as indicators of the diversity of many other, much less well known taxaFthat is, as indicators of the overall biodiversity of a region. Other groups have many of these same attributes but have not gained the same popularity, perhaps because often they are not also large bodied or perceived as being quite so attractive. The list of those that have been advocated as useful biodiversity indicators at one time or another is very long. It includes soil nematodes, moths, beetles galore (tiger, carabid, dung, and buprestid, to name but four), termites, fish, frogs, and snakes. Whatever the group, they must also have one further attributeFnamely, that they genuinely indicate levels of biodiversity or at least some of the components of primary interest. The fact that the scientific literature contains suggestions for so many different possible indicators shows that there is little consensus on the matter. Many have been called, but few are chosen. Why? There are two, related, reasons. First, scientific knowledge on the degree of coincidence in patterns of biodiversity between

different taxa is surprisingly poor. Second, as knowledge improves, coincidence between many taxa turns out to be much worse than people had imagined, or indeed hoped, would be the case.

Knowledge is Poor Because of the Effort Required Gathering information on the diversity of different groups of organisms, even in one place, is enormously time-consuming. Two examples illustrate the problem. To map the presence and absence of breeding birds (conspicuous, ‘‘easy’’ to find and to identify) in every 10 10km grid-square in Britain and Ireland (there are 3672 squares) took more than half a million individual record cards, filled in by an army of amateur birdwatchers coordinated by professional ornithologists in the British Trust for Ornithology (BTO). The task took 4 years and about 100,000 hours of fieldwork (Gibbons et al., 1993). Now imagine the effort required to do the same thing for all the other hundreds of different groups of organisms found in this one small corner of Europe. It has been done for a sample of taxa (we will return to what these data show in a moment), but many groups remain unmapped. At a much smaller spatial scale in a tropical forest in Cameroon, a group of biologists attempted to measure the impacts of forest disturbance on just eight groups (birds, butterflies, flying beetles, canopy beetles, canopy ants, leaflitter ants, termites, and soil nematodes). The birds and the butterflies took 50 and 150 scientist-hours, respectively, to survey. But the effort required climbed rapidly for smallerbodied, more cryptic, less well-known groupsF1600 hours for the beetles, 2000 for the termites, and 6000 for the nematodes (Lawton et al., 1998). Despite the fact that this work as a whole took about five scientist-years, inventories for most groups that were surveyed were still only partial, and most taxa remained unexamined (fungi, higher plants, spiders, soil mites, collembola, earthworms, lizards, frogs, and mammals, to name some of the most conspicuous gaps). Given this background, it is hardly surprising that biologists do not have a complete inventory of all the species that occur even in a single, moderately sized area (a field, small wood, or lake)Fa so-called ATBI (All Taxa Biodiversity Inventory) (Oliver and Beattie, 1996). A moments thought will also show that to use one or two groups (for the sake of the argument, say birds and butterflies) as indicators of the richness of other taxa in fact requires several such areas to be investigated to properly test the hypothesis that high bird diversity (or any other single group) reflects a high diversity of many other groups. Although progress has been made in this area over the past decade, considerable work remains to be done. Even in otherwise well-studied situations, many groups remain to be examined. Hence, at the present time, and effectively by default, some groups are being used as indicators of biodiversity, even though we cannot show categorically that the richness of one or more groups of organisms truly reflects the overall, or even a major portion of the overall, biodiversity of an area. As a result there is little consensus about what a ‘‘good’’ indicator group, or groups, might be, because there are too few hard data, from a range of habitats and geographic regions round

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the world, on which to draw firm conclusions. But as data slowly emerge, they are not encouraging for those who wish to use simple, single-taxon indicators of biodiversity.

Indicator Reliability Where knowledge exists, it suggests that single or small numbers of taxa will usually be poor indicators of the biodiversity of other groups.

Tropical versus Temperate and Other Major Diversity Gradients It would be wrong to think that there is no coincidence between patterns of diversity in different groups of organisms. Of course there is. In the broadest terms, it is axiomatic that most major terrestrial and freshwater groups are more species rich in the tropics than in temperate regions, at low elevations than at high ones, in forests than in deserts, and on large land masses than tiny islands. Whether you are a botanist, a birdwatcher, or a bug hunter, to find the most species it is generally advisable to head to hot and humid mainland tropics with lots of trees. It is easy to assume that there must therefore be reasonably good correlations between major diversity gradients for different groups. There can be, but even at this scale often there are not. Penguin diversity peaks in Antarctica, not the tropics, and there are many other examples of similar ‘‘reverse diversity gradients’’ that buck the average trend. On the eastern side of North America, the diversity of breeding warblers increases from south to northFsuggesting that this conspicuous taxon, which is easy to identify (at least the breeding males!) and to survey, is probably highly unsuitable as an indicator of patterns of biodiversity in most other taxa (in which diversity typically decreases from south to north). In the case of breeding North American warblers, we can spot the problem because we have enough information about the organisms involved. But the whole point about indicator taxa for biodiversity is that typically we will not be armed with, and indeed should not need, information about ‘‘other’’ groups; knowledge of the indicator taxon should suffice and be reliable. The evidence suggests otherwise.

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butterflies. But these correlations are frequently weak, of rather limited predictive value, and in some cases explained by latitudinal gradients in diversity. In other words, although such correlations may sometimes enable a very general impression of the patterns in richness of one group to be obtained from the patterns in richness of another, their predictive powers are low. These conclusions seem to hold at finer resolutions over more constrained areas. Thus, species-rich areas for different taxa in Britain (birds with butterflies, dragonflies, etc.) frequently do not coincide at a scale of 10 10 km squares (Pendergast et al., 1993) (Figure 5). Hot spots in this study are not distributed randomly, overlapping more often than expected by chance, but still at a low level. Likewise, different taxa are species poor or species rich in different areas of the Transvaal region of South Africa. At even finer scales, within the Cameroon forest mentioned earlier, disturbance impacted on the diversity of eight taxa in very different ways. All declined drastically in completely cleared areas, but intermediate levels of forest disturbance had very different effects on the diversity of different groups. As a result, changes in the diversity of one taxon could not be used to predict changes in the diversity of any other (Lawton et al., 1998). A summary of these and related studies showing similar results is provided by Gaston (1996a, 1996b) and by Pimm and Lawton (1998).

A Common Sense Explanation This lack of, or relatively feeble correlation between, species rich-areas for different groups of organisms makes the search for simple, robust, single-taxon indicators of overall biodiversity look increasingly like a lost cause. With hindsight, perhaps this emerging result is obvious (Reid, 1998). Major geographic gradients in biodiversity aside, within particular geographic regions or at smaller habitat scales, the conditions favoring one group of species may be hostile to another. Mollusks like it cool and wet, butterflies like it warm and sunny, and high bird diversity is more likely in tall vegetation than short vegetation, irrespective of weather. Common sense natural history suggests that there is unlikely to be a single indicator taxon able to predict the diversity of all, or even a majority of others.

Hot Spots Major gradients in diversity aside, at similarly large scales an indicator group might be used to identify local geographic hot spots in the species richness of one or more other groups (peaks in the landscape of species richness) or to determine relative levels of richness in those other groups (hot spots versus all spots) (Gaston, 1996b; Reid, 1998). At the continental scale, the procedure has frequently been found to fail on both counts (Gaston, 1996a), with mismatches between the occurrence of peaks in the richness of different groups being commonplace. Across the United States and southern Canada, hot spots (local areas with unusually high diversity) overlap partially between some pairs of taxa (trees, tiger beetles, amphibians, reptiles, birds, and mammals), but the pattern is not a general one. Numbers of species in different large grid cells for two groups are often significantly positively correlated, for example, birds and tiger beetles or mammals and swallowtail

Rare Species and Endemic Species Biologists and conservationists are often interested not only in patterns of species richness but also in the distribution of unusually rare species, or of endemic species. Do sites with unusual numbers of rare species frequently coincide across different taxa? Again, the answer seems to be no, or only weakly (Pimm and Lawton, 1998; Prendergast et al., 1993), for the reasons just outlined. Endemic species may be different (Bibby et al., 1992). There is some evidence that areas rich in endemic birds (e.g., some tropical mountaintops or isolated islands) may also contain unusually large numbers of endemic species in other groups. However, rigorous data and analyses are few, and exceptions are easy to find. Lake Baikal has no endemic birds but supports an exceptionally rich, endemic invertebrate fauna and a unique, endemic freshwater seal.

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Figure 5 Coincidence between hot spots for butterflies and up to seven other taxa in Britain. Hot spots are unusually species-rich sites (here defined as the top 5 percentile in Britain). All of the most species-rich localities in Britain for butterflies lie in southern England. Increasingly dark shading indicates that butterfly hot spots coincide with hot spots for an increasing number of other taxa. Note that many butterfly hot spots are not unusually rich in any other species (open circles) and that only one locality (in southeast England, just in from the coast) is a hot spot for all eight taxa in this particular survey. The other taxa are breeding birds, dragonflies, moths, mollusks, aquatic higher plants, and liverworts (simple plants). Reproduced from Prendergast JR, Quinn RM, Lawton JH, Eversham BC, and Gibbons DW (1993) Rare species, the coincidence of diversity hotspots and conservation strategies. Nature 365: 335–337, with additional data and figure kindly provided by John Prendergast.

Selecting Areas to Conserve Biodiversity: Conservation Planning and Reserve Selection Algorithms Biodiversity Indicators and Conservation The general lack of reliable indicator groups for biodiversity is undoubtedly unfortunate for scientists wishing to understand how life is distributed across the earth; the road to an atlas of biodiversity seems set to be a long one. In practice, it may actually prove somewhat less of a worry for one of the primary motivations in the search for indicators for biodiversityF namely, conservation planning. Networks of national parks and reserves are central planks in conservation, albeit alone they are insufficient to protect all species. Their establishment is one of the obligations placed on Parties to the Convention on Biological Diversity. A primary argument for using indicators of biodiversity is to determine the effectiveness of these protected area networks in capturing biodiversity, and the best ways in which they might be extended, in the face of stiff competition with alternative forms of land use. Although hot spots of species richness coincide weakly for different taxa (see the previous section), if we turn the problem around and look at it from a different angle, an interesting picture emerges. Imagine that conservation priorities in Britain have been set by concentrating just on areas rich in birds (the bird hot spots). (Although the general view of many nations is that the British are mad about birds, the country’s protected area network is not based solely on birds. We use the example simply to illustrate a point.) What we discover is that the hot spots for this one group tend to embrace a high proportion of the total species in other groups. Thus, the hot spots for breeding birds contain 87% of the breeding bird species in Britain, 100% of the butterflies, 92% of the dragonflies, 92% of the liverworts, and 94% of the aquatic plants. A reserve

network established around hot spots for one group does a rather good job of ensuring that most species in other groups find a place in the extended ark of protected sites.

Reserve Selection Algorithms Although this message is encouraging, it turns out that designing conservation networks simply on the basis of levels of species richness is extremely inefficient, at least if the goal is to capture representative samples of all taxa. The same species may occur repeatedly in different richness hot spots for a group. Conservationists do not have unlimited resources, and this duplication wastes money on purchasing, or managing, unnecessary land. On the other hand, some species, particularly the rare ones of primary conservation interest, may not occur in any richness hot spots at all. What is required is to identify those areas that constitute the greatest complementary species richness; the complementary part of an area’s biota consists of those species unrepresented in another biota with which it is being compared. To do this, mathematically minded conservation biologists have developed powerful reserve selection algorithms that help to select sites with maximum efficiency, according to some predetermined criteria (Pressey et al., 1993). The criteria may be to maximize the number of species, rare species, or endemic species in a proposed reserve network, at minimum cost, on a minimum area, closest to existing reserves, or what have you. Echoing the conclusions of the previous section, the question then arises as to whether the patterns of complementarity of one group of organisms are congruent with those of another. The question is a new one, with few studies available to answer it. Across 50 forests of Uganda, which boasts more species for its size than almost any other country

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in Africa, and consistent with our earlier conclusions, there was little spatial congruence in the species richness of woody plants, large moths, butterflies, birds, and small mammals once differences in sampling effort were accounted for. However, sets of forests selected using complementarity determined for single taxa were generally similar to those for all other taxa and hence served to capture well the species richness in all these other groups (Howard et al., 1998). If these results generalize to other parts of the world, they send an encouraging message to conservation managers struggling to identify the best areas to set aside as reserves and parks. It says that a complementary and therefore efficiently selected chain of reserves based on a single indicator taxon (or perhaps two or three indicator taxa) may efficiently capture complementary sets of many other groups as well. Unfortunately, the Ugandan results are not supported by similar studies in the Transvaal, elsewhere in Africa (van Jaarsveld et al., 1998). It may therefore be too soon to assume that we can find simple indicators for complementary reserve sets embracing many taxa as a means of conserving biodiversity.

Conclusions The term ‘‘indicator species’’ has three distinct meanings. They are a species, or group of species, that reflect the biotic or abiotic state of an environment; reveal evidence for, or the impacts of, environmental change; or indicate the diversity of other species, taxa, or entire communities within an area. The uses of indicator species in the first two senses of the word are very similar, differing largely in the fact that to indicate change, organisms need to be sampled more than once in the same place and in the same way. Using organisms to indicate the state of, and changes in, the environment has numerous tried and tested applications, from detecting pollution to monitoring recovery of formerly degraded habitats, at many scales, from local to global. The use of indicator species to predict the diversity of other, unstudied taxa for scientific or conservation reasons is much more contentious and may prove to be impossible with any degree of rigor.

See also: Birds, Biodiversity of. Ecotoxicology. Endemism. Environmental Impact, Concept and Measurement of. Greenhouse Effect. Hotspots. Keystone Species. Paleoecology

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