Biodiversity indicators: the choice of values and measures

Agriculture, Ecosystems and Environment 98 (2003) 87–98

Biodiversity indicators: the choice of values and measures

Peter Duelli∗, Martin K. ObristSwiss Federal Research Institute WSL, Zürcherstrasse 111, CH-8903 Birmensdorf-Zürich, Switzerland

Abstract

Ideally, an indicator for biodiversity is a linear correlate to the entity or aspect of biodiversity under evaluation. Differentmotivations for assessing entities or aspects of biodiversity lead to different value systems; their indicators may not correlate atall. For biodiversity evaluation in agricultural landscapes, three indices are proposed, each consisting of a basket of concordantindicators. They represent the three value systems “conservation” (protection and enhancement of rare and threatened species),“ecology” (ecological resilience, ecosystem functioning, based on species diversity), and “biological control” (diversity ofantagonists of potential pest organisms). The quality and reliability of commonly used indicators could and should be testedwith a three-step approach. First, the motivations and value systems and their corresponding biodiversity aspects or entitieshave to be defined. In a time consuming second step, a number of habitats have to be sampled as thoroughly as possible withregard to one or several of the three value systems or motivations. The third step is to test the linear correlations of a choiceof easily measurable indicators with the entities quantified in the second step. Some examples of good and bad correlationsare discussed.© 2003 Elsevier Science B.V. All rights reserved.

Keywords: Biodiversity; Indicator; Arthropods; Correlate

1. Who needs biodiversity indicators?

National and regional agencies for nature conserva-tion, agriculture, and forestry have to monitor speciesdiversity or other aspects of biodiversity, both beforeand after they spend tax money on subsidies or eco-logical compensation management, with the aim ofenhancing biodiversity (European Community, 1997;Ovenden et al., 1998; Wascher, 2000; Kleijn et al.,2001). Similarly, international, national or regionalnon-governmental organisations (NGOs) may wantto monitor aspects of biodiversity at different levelsand scales (Reid et al., 1993; IUCN, 1994; Cohenand Burgiel, 1997). In scientific research biodiversity

∗ Corresponding author. Tel.:+41-1-739-2376;fax: +41-1-739-2215.E-mail address: [email protected] (P. Duelli).

indicators can be used as quantifiable environmen-tal factors. Since the biodiversity of even a smallarea is far too complex to be comprehensively mea-sured and quantified, suitable indicators have to befound.

Those who are responsible for comparing and eval-uating biodiversity have a strong incentive to choose ascientifically reliable and repeatable indicator, whichinevitably increases costs. The financing agencies usu-ally opt for a financially “reasonable” approach, whichoften results in programmes addressing only essentialwork. The resulting compromises make optimisationof the choice of biodiversity indicators and methodsof fundamental importance.

A recent international electronic conference on bio-diversity indicators (http://www.gencat.es/mediamb/bioind, 2000) has revealed widely differing views onwhy and what to measure and quantify.

0167-8809/$ – see front matter © 2003 Elsevier Science B.V. All rights reserved.doi:10.1016/S0167-8809(03)00072-0

http://www.gencat.es/mediamb/bioind

http://www.gencat.es/mediamb/bioind

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Fig. 1. Provisional domain tree of biodiversity based on the survey of 125 text documents in English (Kaennel, 1998). Concepts used by various authors to define biodiversityare in square boxes, related concepts in rounded boxes. Type and direction of conceptual relationships are indicated by arrows. Synonyms and quasi-synonyms are in italics.

P. Duelli, M.K. Obrist / Agriculture, Ecosystems and Environment 98 (2003) 87–98 89

2. Why is it so difficult to reach a consensus onthe use of biodiversity indicators?

The complexity of all the aspects of the term bio-diversity is illustrated inFig. 1. It is obvious thatno single indicator for biodiversity can be devised.Each aspect of biodiversity requires its own indicator.The difficulties for reaching a consensus on the useof biodiversity indicators are manifold. They implydiffering choices for values and measures, which willbe discussed here more in detail.

Terms such as biodiversity, indicator or index arenot well defined and their use varies between differentcountries and disciplines. Dismissing research findingsor scientific reports simply on the grounds of differingviews on the use of particular terms (semantic discrim-ination) would be counterproductive, but study reportsmust clearly state what is meant by the terms used. Ahelpful review on indicator categories for bioindica-tion is given byMcGeoch (1998).

In this paper, the term indicator is used in the senseof any measurable correlate to the entity to be as-sessed: a particular aspect of biodiversity.

The most promising and convincing indicators ofbiodiversity are measurable portions of the entitythat we consider to represent a target aspect of bio-diversity. The term index is used here in the senseof a scaled measure for one or several concordantindicators.

3. Indicator FOR or FROM biodiversity?

A first major source of misunderstanding is, whetherbiodiversity itself is to be indicated, or whether cer-tain components of biodiversity are used as indica-tors for something else. Until 1990, the search forbioindicators had focussed on indicators of “envi-ronmental health” or ecological processes such asdisturbance, human impact, environmental or globalchange (Hellawell, 1986; Spellerberg, 1991; Meffeand Carroll, 1994; Dufrene and Legendre, 1997).After the world-wide launch of the term biodiversityat the Rio Convention in 1992, there was a suddenand drastic shift in the published literature towardsthe search for indicators of biodiversity itself (Noss,1990; Gaston and Williams, 1993; Gaston, 1996a;Prendergast, 1997). Since then, however, the term

biodiversity has sometimes been used to allude to orindicate some aspect of environmental quality.

If a species or a group of species is a good indicatorfor lead contamination, it may not indicate biodiver-sity, i.e. there may not be a linear correlate to biodi-versity. It is fundamentally a contamination indicator,or an environmental indicator (McGeoch, 1998) ratherthan a biodiversity indicator.

However, “real” biodiversity indicators may beneeded to measure the impact of e.g. lead contami-nation on biodiversity itself (indicator FOR biodiver-sity). Such an assessment is different from measuringthe impact of lead on a selected taxonomic group,which had been chosen because it is especially sensi-tive to lead poisoning (indicator FROM biodiversity).

4. Alpha-diversity, or contribution to higherscale biodiversity?

A second major dichotomy in the value system forbiodiversity indicators is the question of whether thespecies (or allele, or higher taxon unit) diversity of agiven area is to be indicated (local, regional or nationallevel), or if the contribution of the biodiversity of thatarea to a higher scale surface area (regional, national,global) is important.

In the first case (alpha-diversity, e.g. species rich-ness of an ecological compensation area), an indicatorideally has to be a linear correlate to the biodiversityaspect or entity of the surface area in question. Eachspecies has the same value.

In the second case, the value of the measurable unitsof biodiversity (alleles, species, ecosystems) dependson their rarity or uniqueness with regard to a higherlevel area. A nationally rare or threatened species ina local assessment has a higher conservation valuethan a common species, because it contributes moreto regional or national biodiversity than the ubiqui-tous species. Thus a biodiversity indicator in the lattercase not only has to count the units (alleles, species,ecosystems), but it has to value them differently andadd the values.

The best known examples are red list species. Formeasuring alpha-diversity, they are not given a valuethat is greater than any other species in a plot or trapsample, but for measuring the conservation value of aplot, their higher contribution to regional, national, or

90 P. Duelli, M.K. Obrist / Agriculture, Ecosystems and Environment 98 (2003) 87–98

even global biodiversity has to be recognised. Raisedbogs are notorious for their poor species richness,but if only a few raised bogs are left within a coun-try, the few characteristic species present in a “goodbog” are of very high national importance. The prob-lems of estimating complementarity or distinctnessare addressed e.g. byColwell and Coddington (1994)andVane-Wright et al. (1991), endemism and spatialturnover byHarte and Kinzig (1997).

This dichotomy between “species richness” and“conservation value” is the most fervently debatedissue among applied biologists concerned with biodi-versity indicators, and a recurrent source of misunder-standings. It will be elaborated further in the chapteron value systems.

5. Indicator for what aspect of biodiversity?

After agreement on indicators FOR biodiversity,and a decision between “alpha-diversity” and “con-tribution to higher scale biodiversity”, there is stillpotential for disagreement on “what is biodiversity?”(Gaston, 1996c). In practice, in a majority of cases,species are “the units of biodiversity” (Claridge et al.,1997). However, species diversity can be measured assimple number of species, usually of selected groupsof organisms, or species richness may be combinedwith the evenness of the abundance distribution of thespecies. The best known indices are the Shannon in-

Fig. 2. “Which of the two populations do you consider to have a higher biodiversity?” A choice test for biodiversity evaluation regularlyoffered by the first author to students and at public lectures. For the vote, only the upper part without text is shown.

dex, the Simpson index and Fisher’s alpha (Magurran,1988). Recent observations (Duelli, unpubl.) haveshown that when undergraduate biodiversity studentsin entomology lectures have to choose which of thetwo communities shown inFig. 2 (without seeing thetext below them) they consider to be more diverse,more than half of them decide for the left popula-tion, because they consider evenness to be of greaterimportance than species numbers. When individualsfrom other disciplines were asked during lectures andseminars, particularly conservationists and extensionworkers in agriculture and forestry, species numbersare decisive. In recent years, indices involving even-ness have essentially fallen out of favour, mostlybecause they are difficult to interpret (Gaston, 1996c).Particularly in agriculture or forestry, single speciesare often collected in huge numbers with standardisedmethods, which results in a drastic drop of evennessand hence yields low diversity values, in spite ofcomparatively high species richness.

The definition of biodiversity given in the interna-tional Convention on Biological Diversity (Johnson,1993) encompasses the genetic diversity withinspecies, between species, and of ecosystems. Fur-thermore, Noss (1990)distinguished three sets ofattributes: compositional, structural and functionalbiodiversity (see alsoFig. 1). The most common ap-proach is to measure compositional biodiversity. Pre-sumably, both structural and functional biodiversityare either based on or lead to higher compositional


diversity. We are convinced that ecosystem diver-sity, as well as structural and functional diversity, issomehow reflected in the number of species present.If they are not correlated with species richness, theymust be special cases and not representative as biodi-versity indicators. More trophic levels will normallyinclude more species, and a higher structural diversitywill harbour more ecological niches. In fact, there isincreasing evidence that at least for some taxonomicgroups, species numbers are correlated with habitatheterogeneity (Moser et al., 2002), but not in others(Rykken and Capen, 1997).

For all these hierarchical separations or entitieswithin the huge concept of biodiversity, separatecomprehensible indicators can be researched and de-veloped. In many cases, however, a rigorous scientifictest may show that the conceptual entities are difficultto quantify (Prendergast, 1997; Lindenmayer, 1999;Noss, 1999), or they are basically reflected in other,

Fig. 3. Illustration of the hypothesis that abundant species usually are of higher ecological but lower conservation value, in contrast torare and threatened species. Stars indicate red list species collected with pitfall traps, yellow water pans and window interception traps ina semidry meadow (Duelli and Obrist, 1998). Number of individuals (N Ind(log)) are plotted versus number of species (N species).

better quantifiable measures of biodiversity, suchas species richness (Gaston, 1996b; Claridge et al.,1997).

The aspect of intraspecific diversity is a differentcase. To our knowledge there is no published exampleof a tested correlation between inter- and intraspecificdiversity.

6. Value systems

People involved in developing or using biodiversityindicators are influenced by their personal and/or pro-fessional goals. They all may want to measure or mon-itor biodiversity, but they address different aspects ofit. Their focus depends on their motivation for deal-ing with biodiversity. In an agricultural context, andin an industrialised country in Europe, the three mostimportant motivations to enhance biodiversity are


1. Species conservation (focus on rare and endangeredspecies).

2. Ecological resilience (focus on genetic or speciesdiversity).

3. Biological control of potential pest organisms (fo-cus on predatory and parasitoid arthropods).

There are additional motivations, of course, buteither they are closely related to the ones mentionedhere, or their causal link to biodiversity is less clear(e.g. sustainability, landscape protection, culturalheritage).

Each of these three aspects of biodiversity requiresits own indicators. They often do not correlate witheach other or even show a negative correlation. Con-sequently, simply adding up different indicators maylead to misinterpretations, as long as they do not ad-dress the same aspect of biodiversity. Species con-servation focusses on rare and threatened species andoften regards more common species in a derogatoryway as ubiquists of little interest. Ecologists, on theother hand, focus more on abundant species, because aspecies on the verge of extinction is likely to have lesssignificant ecological influence. The hypothesis of analmost vicarious relationship between the motivations

Fig. 4. Neither red list carabid species nor stenotopic carabid species are correlated significantly with the average number of carabid speciescollected in 18 types of habitats using pitfall traps. Data fromFoster et al. (1997).

of “species conservation” and “ecological resilience”is illustrated inFig. 3.

Prendergast et al. (1993)found low coincidence ofspecies-rich areas and areas harbouring rare speciesfor either plants, birds, butterflies or dragonflies. Aninvestigation of carabid beetles in Scotland (Fosteret al., 1997) showed that neither the number of redlist species nor the number of stenotopic (faunisticallyinteresting) species are correlated with the mean totalnumber of carabid species in a variety of habitats suchas moorland, grassland, heathland, peat, saltmarsh,bracken and swamps (Fig. 4). In an intense investiga-tion with 51 trap stations and standardised samplingmethods in field and forest habitats in Switzerland,the number of red list species of all identified arthro-pod groups was not significantly correlated to overallspecies richness per trap station (Fig. 5), while e.g.the numbers of aculeate Hymenoptera species corre-lated well (R2 = 0.88; Fig. 6). In an assessment ofthe effects of ecological compensation measures inSwiss crop fields and grassland, the number of but-terfly species did not show any correlation with thespecies numbers of spiders (Jeanneret, pers. comm.).In an effort to test the suitability of Collembola asindicators of the conservation value of Australian


Fig. 5. No significant correlation exists between the number of red list species (from numerous arthropod taxa) and the “overall” number ofarthropods collected with flight traps, pitfall traps and yellow water pans at the same 51 locations (Araneae, Coleoptera, Diplopoda, Diptera(Syrphidae only), Heteroptera, Hymenoptera (Aculeata only), Isopoda, Mecoptera, Megaloptera, Neuroptera, Raphidioptera, Thysanoptera).Data from agricultural areas (Duelli and Obrist, 1998) and forest edges (Flückiger, 1999).

grasslands,Greenslade (1997)found no correlationwith species numbers of ants and carabid beetles.

The optimal approach is to select a “basket” ofindicators for each motivation, similar to the Dow

Fig. 6. Species numbers of aculeate Hymenoptera (bees, wasps and ants) show excellent correlation with the overall number of arthropodspecies at 51 locations (for details of data sources seeFig. 5).

Jones index for the stock exchange. The measuredindicators within one basket have to be fairly con-cordant and are pooled to form an index. The re-sult is a set of three separate indices for the three


basic motivations “conservation”, “ecology” and “pestcontrol”.

7. How to select indicators for the three mainmotivations

7.1. Several steps are necessary

The most accurate indicators of biodiversity areproven linear correlates of the entity or aspect of biodi-versity being evaluated.McGeoch (1998)proposed anine-step approach for selecting bioindicators amongterrestrial insects. Basically, the whole procedure canbe separated into three steps. The first step is to de-fine the aspect or entity in as quantifiable a way aspossible. The second step is to actually quantify thataspect or entity in a statistically reliable number ofcases. The third step is a rigorous test for linear cor-relation in a set of proposed indicators. The urgentneed to perform a scientifically solid test has been ad-vocated repeatedly (Balmford et al., 1996; McGeoch,1998; Niemelä, 2000).

Starting with the first step, the three mayor motiva-tions for protecting or enhancing biodiversity in agri-cultural landscapes are differentiated.

7.2. Conservation (an index based on the motivationto protect or enhance threatened species)

For assessing the value of a given habitat, e.g.an ecological compensation area, for species con-servation, the entity to indicate is the accumulatedconservation values (e.g. red list status) of all speciespresent in that area. The highest values are contributedby species of national or even global importance,while the so-called ubiquists are of little value. Thesecond step thus is a comprehensive measurement ofthe conservation values in a number of ecosystems orhabitat types.

The third step would be to find and test the bestlinear correlate to that otherwise elusive entity “con-servation value”. The standard indicators for theconservation basket are numbers of red list species ofselected taxa, weighed according to their category ofthreat. However, only very few of the tens of thou-sands of species present in a country are listed; inSwitzerland they are a mere 7% of all known animal

species (Duelli, 1994). Inevitably, the choice of thegroups of organisms used for an inventory dependsstrongly on the red lists available, and on the avail-ability of specialists to identify the listed organisms.

Lacking the information on the second step (fullaccount of the conservation value of an area), it isnot currently possible to come up with a scientificallytested indicator for that value. Nevertheless, a correla-tion between the cumulated conservation values of allpresently available red listed species per habitat withthe conservation values of single taxonomic groups,such as birds, butterflies or carabids, would at leastgive greater credibility to the red list species approach.

In addition to red list status (degree of threat of ex-tinction), species values have been calculated on thebases of national or global rarity (Mossakowski andPaje, 1985) or endemism. The rationale in the contextof habitat evaluation is that the presence of a nation-ally or globally rare species increases the biodiversityvalue of that habitat, because it contributes more tothe conservation of national or global biodiversity thanthe presence of a ubiquitous species.

Only after a reliable basket of indicators for con-servation value has been established, are further stepspossible to test the correlative power of potential in-dicators such as length of hedgerows, amount of deadwood, or the surface of ecological compensation ar-eas per unit area. Environmental diversity (ED) as asurrogate measure of the conservation value was pro-posed byFaith and Walker (1996), but so far there areno empirical data to test their proposal.

7.3. An index for the motivation “pest control”

For the biodiversity aspect of biological control ofpotential pest organisms, the first step may be to de-fine the measurable entity as the species diversity ofall predators or parasites of potential pest organisms.For short-term interests, the number of individuals ofbeneficial organisms may appear more important thanspecies richness, because prey and hosts are reducedby the number of antagonistic individuals rather thanby species numbers (Kromp et al., 1995; Wrattenand Van Emden, 1995). However, with a longer-termperspective on maintaining a high diversity of antag-onist species of potential pest organisms is certainlymore important. While the species richness of preda-tors in a small area can be assessed with reasonable


accuracy and effort, the diversities of parasitoids aremuch harder to quantify.

The second step is therefore to test inventory meth-ods, and selected taxa for their correlation with theabove biodiversity aspect of biological control. Atpresent species numbers of carabid and staphylinidbeetles, as well as spiders, are often used as indica-tors because of established standardised collectingmethods (Duffey, 1974; Desender and Pollet, 1988;Halsall and Wratten, 1988) and readily available keysfor identification and interpretation. Specialised aphi-dophaga among the syrphid flies, coccinellids andNeuroptera are another option, but so far the meth-ods are not fully standardised. Parasitoid wasps andflies are promising, but so far there is no easy way toidentify them to the species level. Other possibilitiesfor indicators to test are ratios between herbivoresand predators, or parasitoids and a range of otherarthropods (see e.g.Denys and Tscharntke, 2002).

7.4. An index for ecological resilience

For the basket of indicators for the motivation eco-logical resilience (“Balance of Nature”,Pimm, 1991),the entire genetic and taxonomic spectrum of biodi-versity is the entity to be indicated. The assumption isthat the higher the number of alleles and species, thehigher is the ecological potential of an ecosystem toreact adequately to environmental change.

Here again, a first step requires quantification ofa measurable proportion of local organismic diver-sity, which can be trusted to represent total speciesrichness of animals and plants (alpha-diversity). Re-alistically, only few and small areas will ever befully assessed. For the second and third steps, ap-proximations with large, measurable proportionsof alpha-diversity have to be used to test potentialindicators.

These “ecological” indicators can be seen as indica-tors for ecosystem functioning (Schläpfer et al., 1999)and are representing a very basic notion of wholesalebiodiversity. Most studies claiming to measure or in-dicate biodiversity assume that the group of organismsthey investigate is somehow representative of biodi-versity. However, in only very few cases has the cor-relation between a group or several groups of specieswith a more or less representative sample of all organ-isms been measured and published (Abensperg-Traun

et al., 1996; Balmford et al., 1996; Cranston andTrueman, 1997; Duelli and Obrist, 1998).

8. Effort and costs, the limiting factors for thechoice of measures

8.1. The dilemma of indicating complexity withsimple measures

Large environmental monitoring programmes usu-ally avoid using invertebrates for their indicators,although these constitute by far the largest portion ofmeasurable biodiversity. To cut down on effort andcosts, measurement of the immense richness and quan-tity of invertebrates has to be reduced to an optimisedselection of taxa. The proposed three-step approachallows for testing all kinds of indicators for their cor-relation with aspects of biodiversity. The search forlinear correlates of quantified entities or aspects ofbiodiversity is not limited to taxonomic units. Insteadof choosing birds or grasshoppers as indicators, thespectrum of taxa considered can be determined by aninventory method such as Berlese soil samples or flightinterception traps. The broader the taxonomic spec-trum of the samples, the higher the chance of obtain-ing a good correlation with the entity to be assessed.Furthermore, indicators, which are not part of the or-ganismic spectrum, can also be tested in the three-stepapproach: habitat diversity and heterogeneity, distur-bance by traffic, neighbourhood or percentage of pro-tected areas, etc. At present, various indicators are inuse, but few of them have been tested for their correla-tion with aspects of biodiversity. At least in Neotropi-cal butterflies, a positive correlation of species richnesswas found with composite environmental indices ofheterogeneity and natural disturbance (Brown, 1997).

8.2. Plots and transects

Plots (for plants) and transects (for birds and in-sects such as butterflies, dragonflies and grasshoppers)are widely used relative assessment methods for thespecies richness of a selected group of organisms (e.g.Pollard and Yates, 1993; Wagner et al., 2000). Themain advantages are that the specimens survive the in-ventory (important for indicating conservation value),and that large areas can be searched in a relatively


short time. Scientifically, the drawback is that usuallythere are no voucher specimens kept for verifying theidentification. Also, these popular groups (except forvascular plants) have only few species in agriculturalhabitats, so their species richness, even if cumulated,never reaches 1% of the local species diversity of allorganisms. Their correlation power with local speciesdiversity has never been tested. Vascular plants, onthe other hand, seem to correlate reasonably well withoverall organismic diversity (Duelli and Obrist, 1998).Plots and transects are low budget measures and worthtesting for their correlation power in the conservationand ecology baskets of indicators.

8.3. Standardised trapping methods for arthropods

Pitfall traps for surface dwelling arthropods and var-ious kinds of flight traps for insects are often usedfor biodiversity assessment in agricultural areas. Ei-ther one or a few taxonomic groups are collected overlonger periods, or a larger number of taxa are sampledwithin a shorter collecting period. In both cases, suit-able correlates have been found for the indicator bas-ket of ecological resilience (Duelli and Obrist, 1998).Bugs (Heteroptera), and wild bees and wasps (ac-uleate Hymenoptera; see alsoFig. 6) collected duringan entire vegetation period, where highly correlatedwith overall species richness, while carabids and spi-ders in pitfall traps were not. Reducing the collectingtime to five carefully selected weeks, but extendingthe spectrum of identified taxa (Duelli et al., 1999),yielded correlation values comparable to those of sea-sonal collections of bugs or bees. Tests are under wayto further reduce the effort required for collecting andidentifying through an adaptation of the Australianmethod of Rapid Biodiversity Assessment (Cranstonand Hillman, 1992; Oliver and Beattie, 1996). Withthat method, the whole taxonomic spectrum collectedwithin a few selected weeks in a standardised trapcombination is considered, but only at the level ofmorphospecies, i.e. without identifying the catchesto the species level (Duelli et al., unpubl.). Obvi-ously, the resulting indicator will not be useful forthe indicator baskets of conservation or pest control,where identification of the species is essential. How-ever, it is a promising monitoring device for the indi-cation of alpha-diversity—or the ecological resiliencebasket.

9. Conclusions

There is no single indicator for biodiversity. Thechoice of indicators depends on the aspect or entity ofbiodiversity to be evaluated and is guided by a valuesystem based on personal and/or professional moti-vation. Each biodiversity index for a particular valuesystem should consist of a basket of methods with oneor several concordant indicators. In order to achievegreater reliability and a broader acceptance, indicatorshave to be tested for their linear correlation with a sub-stantial and quantifiable portion of the entity to assess.The challenge now is to assign all the presently used orproposed indicators to a basket with a declared valuesystem—and to test them with empirical measures.

References

Abensperg-Traun, M., Arnold, G.W., Steven, D.E., Smith, G.T.,Atkins, L., Viveen, J.J., Gutter, M., 1996. Biodiversity indicatorsin semiarid, agricultural Western Australia. Pacific Conserv.Biol. 2, 375–389.

Balmford, A., Green, M.J.B., Murray, M.G., 1996. Usinghigher-taxon richness as a surrogate for species richness. I.Regional tests. Proc. R. Soc. Lond. B 263, 1267–1274.

Brown, K.S., 1997. Diversity, disturbance and sustainable useof Neotropical forests: insects as indicators for conservationmonitoring. J. Insect Conserv. 1, 25–42.

Claridge, M.F., Dawah, H.A., Wilson, M.R. (Eds.), 1997. Species:The Units of Biodiversity. Chapman & Hall, London.

Cohen, S., Burgiel, S.W. (Eds.), 1997. Exploring BiodiversityIndicators and Targets under the Convention on BiologicalDiversity. BIONET and IUCN, Washington, DC and Gland.

Colwell, R.K., Coddington, J.A., 1994. Estimating terrestrialbiodiversity through extrapolation. Phil. Trans. R. Soc. Lond.B 345, 101–118.

Cranston, P.S., Hillman, T., 1992. Rapid assessment of biodiversityusing biological diversity technicians. Aust. Biol. 5, 144–154.

Cranston, P.S., Trueman, J.W.H., 1997. Indicator taxa ininvertebrate biodiversity assessment. Mem. Mus. Victoria 56,267–274.

Denys, C., Tscharntke, T., 2002. Plant–insect communities andpredator–prey ratios in field margin strips, adjacent crop fields,and fallows. Oecologia 130, 315–324.

Desender, K., Pollet, M., 1988. Sampling pasture carabids withpitfalls: evaluation of species richness and precision. Med. Fac.Landbouww. Rijksuniv. Gent 53, 1109–1117.

Duelli, P., 1994. Rote Listen der gefährdeten Tierarten der Schweiz.Bundesamt für Umwelt Wald und Landschaft. BUWAL-ReiheRote Listen. EDMZ, Bern.

Duelli, P., Obrist, M.K., 1998. In search of the best correlatesfor local organismal biodiversity in cultivated areas. Biodivers.Conserv. 7, 297–309.


Duelli, P., Obrist, M.K., Schmatz, D.R., 1999. Biodiversityevaluation in agricultural landscapes: above-ground insects.Agric. Ecosyst. Environ. 74, 33–64.

Duffey, E., 1974. Comparative sampling methods for grasslandspiders. Bull. Br. Arach. Soc. 3, 34–37.

Dufrene, M., Legendre, P., 1997. Species assemblages and indicatorspecies: the need for a flexible asymmetrical approach. Ecol.Monogr. 67, 345–366.

European Community, 1997. Agenda 2000, vol. L, For a Strongerand Wider EU. Office for Official Publications of the EuropeanCommunities, Luxembourg.

Faith, D.P., Walker, P.A., 1996. Environmental diversity: on thebest-possible use of surrogate data for assessing the relativebiodiversity of sets of areas. Biodivers. Conserv. 5, 399–415.

Flückiger, P.F., 1999. Der Beitrag von Waldrandstrukturenzur regionalen Biodiversität. Doctoral Thesis. Philosophisch-Naturwissenschaftliche Fakultät, Universität Basel, Basel.

Foster, G.N., Blake, S., Downie, I.S., McCracken, D.I., Ribera,I., Eyere, M.D., Garside, A., 1997. Biodiversity in Agriculture.Beetles in Adversity? BCPC Symposium Proceedings No. 69:Biodiversity and Conservation in Agriculture, pp. 53–63.

Gaston, K.J. (Ed.), 1996a. Biodiversity: A Biology of Numbersand Difference. Blackwell Scientific Publications, London.

Gaston, K.J. (Ed.), 1996b. Species Richness: Measure andMeasurement. Biodiversity: A Biology of Numbers andDifference. Blackwell Scientific Publications, London.

Gaston, K.J. (Ed.), 1996c. What is Biodiversity? Biodiversity:A Biology of Numbers and Difference. Blackwell ScientificPublications, London.

Gaston, K.J., Williams, P.H., 1993. Mapping the world’s species—the higher taxon approach. Biodiv. Lett. 1.

Greenslade, P., 1997. Are Collembola useful as indicators of theconservation value of native grassland? Pedobiologia 41, 215–220.

Halsall, N.B., Wratten, S.D., 1988. The efficiency of pitfall trappingfor polyphagous predatory Carabidae. Ecol. Entomol. 13, 293–299.

Harte, J., Kinzig, A., 1997. On the implications of species–arearelationships for endemism, spatial turnover, and food webpatterns. Oikos 80, 417–427.

Hellawell, J.M., 1986. Biological Indicators of FreshwaterPollution and Environmental Management. Elsevier, London.

IUCN, 1994. IUCN Red List Categories. Prepared by IUCNSpecies Survival Commission. IUCN, Gland.

Johnson, S.P., 1993. The Earth Summit: The United NationsConference on Environment and Development (UNCED).Graham and Trotman, London.

Kaennel, M., 1998. Biodiversity: a diversity in definition. In:Bachmann, P., Köhl, M., Päivinen, R. (Eds.), Assessment ofBiodiversity for Improved Forest Planning. Kluwer AcademicPublishers, Dordrecht.

Kleijn, D., Berendse, F., Smit, R., Gilissen, N., 2001. Agri-environment schemes do not effectively protect biodiversity inDutch agricultural landscapes. Nature 413, 723–725.

Kromp, B., Pflügel, G., Hradetzky, R.I.J., 1995. Estimatingbeneficial arthropod densities using emergence traps, pitfalltraps and the flooding method in organic fields (Vienna,

Austria). In: Toft, S., Riedel, W. (Eds.), Arthropod NaturalEnemies in Arable Land, vol. 70. Acta Jutlandica, AarhusUniversity Press, Denmark, Aarhus, Denmark, pp. 87–100.

Lindenmayer, D.B., 1999. Future directions for biodiversityconservation in managed forests: indicator species, impactstudies and monitoring programs. For. Ecol. Manage. 115, 277–287.

Magurran, A.E., 1988. Ecological Diversity and its Measurement.Croom Helm Limited, London.

McGeoch, M.A., 1998. The selection, testing and application ofterrestrial insects as bioindicators. Biol. Rev. 73, 181–201.

Meffe, G.K., Carroll, C.R., 1994. Principles of ConservationBiology. Sinauer, Sunderland.

Moser, D., Zechmeister, H.G., Plutzar, C., Sauberer, N., Wrbka, T.,Grabherr, G., 2002. Landscape patch shape complexity as aneffective measure for plant species richness in rural landscapes.Landscape Ecol. 17, 657–669.

Mossakowski, D., Paje, F., 1985. Ein Bewertungsverfahren vonRaumeinheiten an Hand der Carabidenbestände. Verh. Ges.Ökol. Bremen 13, 747–750.

Niemelä, J., 2000. Biodiversity monitoring for decision-making.Ann. Zool. Fenn. 37, 307–317.

Noss, R.F., 1990. Indicators for monitoring biodiversity: ahierarchical approach. Conserv. Biol. 4, 355–364.

Noss, R.F., 1999. Assessing and monitoring forest biodiversity: asuggested framework and indicators. For. Ecol. Manage. 115,135–146.

Oliver, I., Beattie, A.J., 1996. Invertebrate morphospecies assurrogates for species: a case study. Conserv. Biol. 10, 99–109.

Ovenden, G.N., Swash, A.R.H., Smallshire, D., 1998. Agri-environment schemes and their contribution to the conservationof biodiversity in England. J. Appl. Ecol. 35, 955–960.

Pimm, S.L., 1991. The balance of nature? Ecological Issues inthe Conservation of Species and Communities. University ofChicago Press, Chicago.

Pollard, E., Yates, T.J., 1993. Monitoring Butterflies for Ecologyand Conservation. Chapman & Hall, London.

Prendergast, J.R., 1997. Species richness covariance in higher taxa:empirical tests of the biodiversity indicator concept. Ecography20, 210–216.

Prendergast, J.R., Quinn, R.M., Lawton, J.H., Eversham, B.C.,Gibbons, D.W., 1993. Rare species, the coincidence of diversityhotspots and conservation strategies. Nature 365, 335–337.

Reid, W.V., McNeely, J.A., Tunstall, D.B., Bryant, D.A., Winograd,M., 1993. Biodiversity Indicators for Policy-makers. WRI andIUCN, Washington, DC and Gland.

Rykken, J.J., Capen, D.E., Mahabir, S.P., 1997. Ground beetlesas indicators of land type diversity in the Green Mountains ofVermont. Conserv. Biol. 11, 522–530.

Schläpfer, F., Schmid, B., Seidl, I., 1999. Expert estimates abouteffects of biodiversity on ecosystem processes and services.Oikos 84, 346–352.

Spellerberg, I.F., 1991. Monitor Ecological Change. CambridgeUniversity Press, Cambridge.

Vane-Wright, R.I., Humphries, C.J., Williams, P.H., 1991. What toprotect?—systematics and the agony of choice. Biol. Conserv.55, 235–254.


Wagner, H.H., Wildi, O., Ewald, K.C., 2000. Additive partitioningof plant species diversity in an agricultural mosaic landscape.Landscape Ecol. 15, 219–227.

Wascher, D.W., 2000. Agri-environmental indicators forsustainable agriculture in Europe. ECNC Technical ReportSeries, Tilburg.

Wratten, S.D., Van Emden, H.F., 1995. Habitat management forenhanced activity of natural enemies of insect pests. In: Glen,D.M., Greaves, M.P., Anderson, H.M. (Eds.), Ecology andIntegrated Farming Systems. Wiley, Bristol.

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Biodiversity indicators: the choice of values and measures