Essay

Indicators for Monitoring : A Hierarchical Approach

REED F. NOSS* US. Environmental Protection Agency Environmental Research Laboratory Corvallis, OR 97333, U.S.A.

Abstract: Biodiversity is presently a minor consideration in Resumen: La biodiversidad es basta ahora una consid- environmentalpolicy. It has been regarded as too broad and eracion menor en lapolitica ambiental. Se ha visto como un vague a concept to be applied to real-world regulatoy and concepto demasiado amplio y vago para ser aplicado en las managernentproblems. Thisproblem can be corrected ifbio- regulacionesy el manejo de losproblemas del mundo real. diversity is recognized as an end in itsea and if measurable Este problema se puede cowegir si la biodiversidad es re- indicators can be selected to assess the status of biodiversity conocida como un fin por si mismu, y si se pueden seleccio- over time. Biodiversity, as presently understood, encom- nar indicadores cuantificables para determinar el estado de passes multiple levels of biological organization. In thispa- la biodiversidad a haves del tiempo. La biodiversidd como per, I expand the three primay attributes of biodiversity se entiende actualmente comprende multiples niveles de or- recognized by Jerry Franklin - composition, structure, and ganizacion biologica En esta disertacion, extiendo 10s tres function - into a nested hierarcby that incorporates ele- atributos primarios de la biodiversidad reconocidos por ments of each attribute at four levels of organization: re- Jerry Franklin - composici6n, estructura y funcion - gional landscape, -, population- dentro de una jerarquia que encaja a incorpora 10s elemen- species, andgenetic. Indicators of each attribute in terrestrial tos de cada uno de 10s atributos en cuatro niveles de orga- , at the four levels of organization, are identified nizaciom paisaje regional, ecosistemas de las comunidades, for environmental monitoring purposes. Projects to monitor poblacion de especies y genbtica Los indicadores de cada biodiversity will benefit from a direct linkage to long-term atributo en 10s ecosistemas terrestres, en 10s cuatro niveles de ecological research and a commitment to test hypotheses organizacion, son identificados para propositos de moni- relevant to biodiversity conservation. A general guideline is tore0 ambiental. Los proyectos para el monitoreo de la bio- to proceed from the top down, beginning with a coarse-scale diversidad se beneficiarian de una union directa con la in- invent0y of landscapepattern, vegetation, structure, vestigacion ecol6gica a laqo plazo y de un compromiso and species distributions, then overlaying data on stress lev- para probar hipotesis relevantes a la consmacidn de la bio- els to identiD biologically significant areas at high risk of diversidact. Un lineamiento general es proceder de awiba impoverishment. Intensive research and monitoring can be para abajo, empezando con una escala-burdade inventario directed to high-risk ecosystems and elements of biodiversity, de lospatrones delpaisaje, de la vegetacion, de la estructura while less intensive monitoring is directed to the total land- del habitat y de la distribucion de Is especies, despds super- scape (or samples thereon. In any monitoringprogram, par- poner 10s datos sobre niveles de presion para identijicar las ticular attention should be paid to specifying the questions areas da alto riezgo y de empobrecimiento.La investigacion that monitoring is intended to answer and validating the intensiva y el monitorio peude ser dirigido a 10s ecosistemas relationships between indicators and the components of bio- de alto riezgo y a 10s elementos de la biodiversidcul;mientras diversity they represent que un monitoreo mhos intenso sepuede dirigir a1 total del paisaje (0 a muestras del mismo). En cualquierprogramu de monitoreo, se debe deponer atencidn especial a1 estar espe- Paper submitted August 22, 1989;revised manuscript accepted No- cificando las preguntas que el monitoreo pretende resolvery oember29, 1989. a1 estar validando las relaciones entre 10s indicadores y 10s ' Current address is 925 N W. 3lst Street, Corvallis, OR 47330 componentes de la biodiversidad que representen.

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Introduction cies, ecosystems, or any other group of things in a de- fined area. Knowing that one community contains 500 Biological diversity (biodiversity) means different species and another contains 50 species does not tell us things to different people. To a systematist, it might be much about their relative importance for conservation the list of species in some taxon or group of taxa. A purposes. Ecologists usually define “diversity” in a way geneticist may consider allelic diversity and heterozy- that takes into consideration the relative frequency or gosity to be the most important expressions of biodi- of each species or other entity, in addition to versity, whereas a community ecologist is more inter- the number of entities in the collection. Several differ- ested in the variety and distribution of species or ent indices, initially derived from information theory, vegetation types. To a wildlife manager, managing for combine richness with a measure of evenness of relative biodiversity may mean interspersing to maxi- abundances (e.g., Shannon & Weaver 1949; Simpson mize , thereby building populations of pop- 1949). Unfortunately, the number of indices and inter- ular game species. Some nonbiologists have complained pretations proliferated to the point where species diver- that biodiversity is just another “smokescreen”or envi- sity was in danger of becoming a “nonconcept” (Hurl- ronmentalist ploy to lock up land as wilderness. No bert 1971). Diversity indices lose information (such as wonder agencies are having difEculty defining and im- species identity), are heavily dependent on sample size, plementing this new buzzword in a way that satisfies and generally have fallen out of favor in the scientific policy-makers, scientists, and public user groups alike. community. As Pielou (1975:165) noted, “a communi- Conservation biologists now recognize the biodiver- ty’s is merely a single descriptive statis- sity issue as involving more than just or tic, only one of the many needed to summarize its char- endangered species. The issue is grounded in a concern acteristics, and by itself, not very informative.” Despite about biological impoverishment at multiple levels of such warnings, diversity indices still are used in mislead- organization. Increasingly, the American public sees bio- ing ways in some environmental assessments (Noss & diversity as an environmental end point with intrinsic Harris 1986). value that ought to be protected (Nash 1989). The Agencies prefer to promulgate and enforce regula- heightened interest in biodiversity presents an oppor- tions based on quantitative criteria, even though quali- tunity to address environmental problems holistically, tative changes in community structure are often the rather than in the traditional and fragmentary species- best indicators of ecological disruption. When a natural by-species, stress-by-stressfashion. One way to escape landscape is fragmented, for example, overall commu- the vagueness associated with the biodiversity issue is to nity diversity may stay the same or even increase, yet identlfy measurable attributes or indicators of biodiver- the integrity of the community has been compromised sity for use in environmental inventory, monitoring, and with an invasion of weedy species and the loss of species assessment programs. The purpose of this paper is to unable to persist in small, isolated patches of habitat provide a general characterization of biodiversity and to (Noss 1983). Qualitative changes at local and regional suggest a set of indicators and guidelines by which bio- scales correspond to a homogenization of floras and fau- diveristy can be inventoried and monitored over time. I nas. As a biogeographical region progressively loses its emphasize terrestrial systems, but many of the guide- character, global biodiversity is diminished (Mooney lines apply to aquatic and marine realms. 1988).

Defining and Characterizing Biodiversity A Hierarchical Characterization of Biodiversity A definition of biodiversity that is altogether simple, What It Is and What It Is Not comprehensive, and fully operational (i.e., responsive to A widely cited definition of biological diversity is “the real-life management and regulatory questions) is un- variety and variability among living organisms and the likely to be found. More useful than a definition, per- ecological complexes in which they occur” (OTA haps, would be a characterization of biodiversity that 1987). The OTA document described diversity at three identifies the major components at several levels of or- fundamental levels: , species diver- ganization. This would provide a conceptual framework sity, and genetic diversity. These three kinds of biodi- for identlfying specific, measurable indicators to moni- versity were noted earlier by Norse et al. (1986). Un- tor change and assess the overall status of biodiversity. fortunately, most definitions of biodiversity, including Franklin et al. ( 1981) recognized three primary at- OTA’s, fail to mention processes, such as interspecific tributes of ecosystems: composition, structure, and interactions, natural disturbances, and nutrient cycles. function. The three attributes determine, and in fact Although ecological processes are as much abiotic as constitute, the biodiversity of an area. Composition has biotic, they are crucial to maintaining biodiversity. to do with the identity and variety of elements in a Biodiversity is not simply the number of genes, spe- collection, and includes species lists and measures of

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species diversity and genetic diversity. Structure is the sessment be limited to higher levels (e.g., remote sens- physical organization or pattern of a system, from hab- ing of regional landscape structure). Lower levels in a itat complexity as measured within communities to the hierarchy contain the details (e.g., species identities and pattern of patches and other elements at a landscape abundances) of interest to conservationists, and the scale. Function involves ecological and evolutionary mechanistic basis for many higher-order patterns. processes, including gene flow, disturbances, and nutri- The hierarchy concept suggests that biodiversity be ent cycling. Franklin (1988) noted that the growing monitored at multiple levels of organization, and at mul- concern over compositional diversity has not been ac- tiple spatial and temporal scales. No single level of or- companied by an adequate awareness of structural and ganization (e.g., gene, population, community) is funda- functional diversity. Hence, structural simplification of mental, and different levels of resolution are appropriate ecosystems and disruption of fundamental ecological for different questions. Big questions require answers processes may not be fully appreciated. Here, I elabo- from several scales. If we are interested in the effects of rate Franklin’s three attributes of biodiversity into a climate change on biodiversity, for instance, we may nested hierarchy (Fig. 1). Because the compositional, want to consider (1) the climatic factors controlling structural, and functional aspects of nature are interde- major vegetation and patterns of species rich- pendent, the three spheres are interconnected and ness across continents; (2) the availability of suitable bounded by a larger sphere of concern (i.e., Earth). habitats and landscape linkages for species migration; Hierarchy theory suggests that higher levels of orga- (3) the climatic controls on regional and local distur- nization incorporate and constrain the behavior of bance regimes; (4)the physiological tolerances, auteco- lower levels (Allen & Starr 1982; O’Neill et al. 1986). If logical requirements, and dispersal capacities of individ- a big ball (e.g., the biosphere) rolls downhill, the little ual species; and (5) the genetically controlled variation balls inside it will roll downhill, also. Hence, global within and between populations of a species in response problems such as greenhouse warming and strato- to climatic variables. “Big picture” research on global spheric ozone depletion impose fundamental con- phenomena is complemented by intensive studies of the straints on efforts to preserve particular natural areas or life histories of organisms in local environments. endangered species. The importance of higher-order Another value of the hierarchy concept for assessing constraints should not suggest that monitoring and as- biodiversity is the recognition that effects of environ- mental stresses will be expressed in different ways at different levels of biological organization. Effects at one level can be expected to reverberate through other lev- els, often in unpredicatable ways. Tree species, for ex- ample, are known to be differentially susceptible to air , with some (e.g.,Pinusponderosa) highly sen- sitive to photochemical oxidants such as ozone (Miller 1973). Different genotypes within tree species vary in their tolerance of air pollution. A decline in a tree pop- ulation due to air pollution would alter the genetic com- position of that population, and reduce genetic varia- tion, as pollution-intolerant genotypes are selected out (Scholz 1981 ). If a declining tree species is replaced by species that are either more or less pyrogenic, or oth- erwise regulatory of dynamics, changes in biodiversity could be dramatic as the system shifts abruptly to a new stable state.

Selecting Biodiversity Indicators Why Indicators? Figure 1. Compositional, structural, and functional Indicators are measurable surrogates for environmental biodiversity, shown as interconnected spheres, each end points such as biodiversity that are assumed to be of encompassing multiple levels of organization. This value to the public. Ideally, an indicator should be ( 1) conceptual framework may facilitate selection of sufficiently sensitive to provide an early warning of indicators that represent the many aspects of biodi- change; (2) distributed over a broad geographical area, versity that warrant attention in environmental or otherwise widely applicable;(3) capable of providing monitoring and assessment programs. a continuous assessment over a wide range of stress; (4)

Conservation Biology Volume 4, No. 4, December I990 358 Indicators for Biodiversiity Noss relatively independent of sample size; (5) easy and cost- itself, rather than as an index of air quality, water quality, effective to measure, collect, assay, and/or calculate; (6) or some other anthropocentric measure of environmen- able to differentiate between natural cycles or trends tal health. (2) Selection of indicators depends on for- and those induced by anthropogenic stress; and (7) rel- mulating specific questions relevant to management or evant to ecologically significant phenomena (Cook policy that are to be answered through the monitoring 1976; Sheehan 1984; Munn 1988). Because no single process. (3) Indicators for the level of organization one indicator will possess all of these desirable properties, a wishes to monitor can be selected from levels at, above, set of complementary indicators is required. or below that level. Thus, if one is monitoring a popu- The use of indicator species to monitor or assess en- lation, indicators might be selected from the landscape vironmental conditions is a firmly established tradition level (e.g., habitat corridors that are necessary to allow in , , pollution control, dispersal), the population level (e.g., , agriculture, forestry, and wildlife and range manage- fecundity, survivorship, age and sex ratios), the level of ment (Thomas 1972; Ott 1978; Cairns et al. 1979). But individuals (e.g., physiological parameters), and the ge- this tradition has encountered many conceptual and netic level (e.g., heterozygosity). (4) The indicators in procedural problems. In toxicity testing, for example, Table 1 are general categories, most of which cut across the usual assumption that responses at higher levels of ecosystem types. In application, many indicators will be biological organization can be predicted by single- specific to ecosystems. Coarse woody debris, for exam- species toxicity tests is not supportable (Cairns 1983). ple, is a structural element critical to biodiversity in Landres et al. (1988) pointed out a number of difficul- many old-growth forests, such as in the Pacific North- ties with using indicator species to assess population west (Franklin et al. 198l), but may not be important in trends of other species and to evaluate overall wildlife more open-structured habitats, including forest types habitat quality, and noted that the ecological criteria subject to frequent fire. used to select indicators are often ambiguous and falli- ble. Regional Landscape Recent criticisms of the use and even the concept of indicator species are valid. Indicator species often have The term “regional landscape” (Noss 1983) emphasizes told us little about overall environmental trends, and the spatial complexity of regions. “Landscape” refers to may even have deluded us into thinking that all is well “a mosaic of heterogeneous land forms, vegetation with an environment simply because an indicator is types, and land uses” (Urban et al. 1987). The spatial thriving. These criticisms apply, however, to a much scale of a regional landscape might vary from the size of more restricted application of the indicator concept a national forest or park and its surroundings up to the than is suggested here. The final recommendation of size of a physiographic region or biogeographic prov- Landres et al. (1988) is to use indicators as part of a ince (say, from lo2 to 10’ h2). comprehensive strategy of risk analysis that focuses on The relevance of landscape structure to biodiversity key habitats (including corridors, mosaics, and other is now well accepted, thanks to the voluminous litera- landscape structures) as well as species. Such a strategy ture on (eg, Burgess & Sharpe might include monitoring indicators of compositional, 1981; Harris 1984;Wilcove et al. 1986). Landscape fea- structural, and functional biodiversity at multiple levels tures such as patch size, heterogeneity, perimeter-area of organization. ratio, and connectivity can be major controllers of spe- cies composition and abundance, and of population vi- An Indicator Selection Matrix ability for sensitive species (Noss & Harris 1986). Re- lated features of landscape composition (i.e., the Table 1 is a compilation of terrestrial biodiversity indi- identity and proportions of particular habitats) are also cators and inventory and monitoring tools, arranged in a critical. The “functional combination” of habitats in the four-level hierarchy. As with most categorizations, some landscape mosaic is vital to that utilize multiple boxes in Table 1 overlap, and distinctions are somewhat habitat types and includes ecotones and species assem- arbitrary. The table may be useful as a framework for blages that change gradually along environmental gradi- selecting indicators for a biodiversity monitoring proj- ents; such gradient-associated assemblages are often ect, or more immediately, as a checklist of biodiversity rich in species but are not considered in conventional attributes to consider in preparing or reviewing envi- vegetation analysis and community-level conservation ronmental impact statements or other assessments. (Noss 1987) Four points about choosing indicators deserve em- The indicators listed for the regional landscape level phasis. (1) The question “What are we monitoring or in Table 1 are drawn mostly from the literature of land- assessing, and why?” is fundamental to selecting appro- scape ecology and disturbance ecology. General refer- priate indicators. I assume that the purpose is to assess ences include Risser et al. (1984), Pickett and White biodiversity comprehensively and as an end point in (1985), and Forman and Godron (1986). O’Neill et al.

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Table 1. Indicator variables for inventorying, monitoring, and assessing terrestrial biodiversity at four levels of organization, including compositional, structural, and functional components; includes a sampling of inventory and monitoring tools and techniques. Indicators Invaztoty and Composition Structure Function monitoring tools

Regional Identity, distribution, Heterogeneity; connectivity; Disturbance processes (areal Aerial photographs (satellite Landscape richness, and proportions spatial linkage; patchiness; extent, frequency or and conventional aircraft) of patch (habitat) types porosity; contrast; grain return interval, rotation and other remote sensing and multipatch landscape size; fragmentation; period, predictability, data; Geographic types; collective patterns configuration; intensity, severity, Information System (GIS) of species distributions juxtaposition; patch size seasonality); nutrient technology; time series (richness, ) frequency distribution; cycling rates; analysis; spatial statistics; perimeter-area ratio; rates; patch persistence mathematical indices (of pattern of habitat layer and turnover rates; rates pattern, heterogeneity, distribution of erosion and connectivity, layering, geomorphic and diversity, edge, hydrologic processes; morphology, human land-use trends autocorrelation, fractal dimension) Comrnunity- Identity, relative abundance, Substrate and soil variables; and Aerial photographs and Ecosystem frequency, richness, slope and aspect; ; herbivory, other remote sensing data; evenness, and diversity of vegetation biomass and , and ground-level photo species and guilds; physiognomy; foliage rates; colonization and stations; time series proportions of endemic, density and layering; local extinction rates; analysis; physical habitat exotic, threatened, and horizontal patchiness; (fine-scale measures and resource endangered species; canopy openness and gap disturbance processes), inventories; habitat -diversity proportions; abundance, nutrient cycling rates; suitability indices (HSI, curves; life-form density, and distribution human intrusion rates and multispecies); proportions; similarity of key physical features intensities observations, censuses and coefficients; C4:C3 (e.g., cliffs, outcrops, inventories, captures, and species ratios sinks) and structural other sampling elements (snags, down methodologies; logs); water and resource mathematical indices (e.g., (e.g., mast) availability; of diversity, heterogeneity, snow cover layering dispersion, biotic integrity) Population. Absolute or relative Dispersion Demographic processes Censuses (observations, Species abundance; frequency; (microdistribution); range (fertility, rate, counts, captures, signs, importance or cover ( macrodistribution); survivorship, mortality); radio-tracking);remote value; biomass; density population structure (sex dynamics; sensing; habitat suitability ratio, age ratio); habitat population genetics (see index (HSI); variables (see below); population species-habitat modeling; community-ecosystem fluctuations; physiology; population viability structure, above); lie history; phenology; analysis within-individual growth rate (of morphological variability individuals); acclimation; adaptation Genetic Allelic diversity; presence of Census and effective Inbreeding depression; Electrophoresis; karyotypic particular rare alleles, population size; outbreeding rate; rate of analysis; DNA sequencing; deleterious recessives, or heterozygosity; genetic drift; gene flow; offspring-parent karyotypic variants chromosomal or mutation rate; selection regression; sib analysis; phenotypic polymorphism; intensity morphological analysis generation overlap; heritabilitv

(1988) developed and tested three indices of landscape regimes. Statistical techniques applicable to landscape pattern, derived from information theory and fractal ge- pattern analysis were summarized by Risser et al. ometry and found them to capture major features of (1984) and Forman and Godron (1986). landscapes. Landscape structure can be inventoried and Monitoring landscape composition requires more in- monitored primarily through aerial photography and tensive ground-truthing than monitoring structure, as satellite imagery, and the data organized and displayed the dominant species composition of patch types (and, with a Geographical Information System (GIs). Time perhaps, several vertical layers) must be identified. series analysis of remote sensing data and indices of Landscape function can be monitored through attention landscape pattern is a powerful monitoring technique. to disturbance-recovery processes and to rates of bio- Monitoring the positions of ecotones at various spatial geochemical, hydrologic, and energy flows. For certain scales may be particularly useful to track vegetation re- ecosystems, such as longleaf pine-wiregrass communi- sponse to climate change and disruptions of disturbance ties in the southeastern United States, a disturbance

Conservation Biology Volume 4, No. 4, December 1990 360 Indicators for Biodiversiry Nos measure as simple as fire frequency and seasonality may cling rates) that may be appropriate to monitor for spe- be one of the best indicators of biodiversity. If fires cialized purposes. occur too infrequently, or outside of the growing sea- Tools and techniques for monitoring biodiversity at son, hardwood trees and shrubs invade, floristic diver- the community-ecosystem level of organization are sity may decline, and key species may be eliminated nearly as diverse as the taxa and systems of concern. (Noss 1988). In many landscapes, human land-use indi- Plant ecology texts (e.g., Greig-Smith 1964; Mueller- cators (both structural and functional: e.g., deforestation Dombois & Ellenberg 1974) contain much information rate, road density, fragmentation or edge index, grazing on community-levelsampling methodology. A tremen- and agricultural intensity, rate of housing development) dous literature exists on census techniques, the and the protection status of managed lands may be the most complete single reference being Ralph and Scott most critical variables for tracking the status of biodi- ( 1981). Bird community data can be readily applied versity. to environmental evaluations (e.g., Graber & Graber In addition to strictly landscape-level variables, col- 1976). Long-term bird surveys across the United States, lective properties of species distributions can be inven- such as the U.S. Fish and Wildlife Service’sBreeding Bird toried at the regional landscape scale. Terborgh and Survey (BBS) program (Robbins et al. 1986), are used to Winter (1983), for example, mapped the distribution of monitor temporal trends in species populations, but endemic land in Columbia and Ecuador and iden- could be interpreted to monitor guilds or the entire tified areas of maximum geographic overlap where pro- avian community of a defined area. Small mammal, rep- tection efforts should be directed. Scott et al. (1990) tile, and monitoring are discussed in several developed a methodology to identlfy centers of species papers in Szaro et al. (1988). Useful summaries of wild- richness and endemism, and vegetative diversity, at a life habitat inventory and monitoring are in Thomas scale of 1:100,000 to 1:500,000,and to identlfy gaps in (1979), Verner et al. (1986), and Cooperrider et al. the distribution of protected areas. In most cases, re- (1986). Karr’s index of biotic integrity (IBI; Karr et al. peating extensive inventories of species distributions 1986), which collapses data on community composition would be impractical for monitoring purposes. Periodic into a quantitative measure, has been applied with suc- inventories of vegetation from remove sensing, how- cess to aquatic communities, and terrestrial applications ever, can effectively monitor the availability of habitats are possible (J. R. Karr, personal communication). over broad geographic areas. Inferences about species distributions can be drawn from such inventories. Population-Species

Community-Ecosystem Monitoring at the species level might target all popula- tions of a species across its range, a metapopulation A community comprises the populations of some or all (populations of a species connected by dispersal), or a species coexisting at a site. The term “ecosystem” in- single, disjunct population. The population-specieslevel cludes abiotic aspects of the environment with which is where most biodiversity monitoring has been fo- the biotic community is interdependent. In contrast to cused. Although the indicator species approach has the higher level of regional landscape, the community- been criticized for its questionable assumptions, meth- ecosystem level is relatively homogenous when viewed, odological deficiencies, and sometimes biased applica- say, at the scale of a conventional aerial photograph. tion, single species will continue to be important foci of Thus, monitoring at this level or organization must rely inventory, monitoring, and assessment efforts, for two more upon ground-level surveys and measurements basic reasons: ( 1) species are often more tangible and than on remote sensing (although the latter is still useful easy to study than communities, landscapes, or genes; for some habitat components). (2) laws such as the U.S. Endangered Species Act (ESA) Indicator variables for the community-ecosystem mandate attention to species but not to other levels of level (Table 1) include many from community ecology, organization (except that the ESA is supposed to “pro- such as and diversity, dominance- vide a means whereby the ecosystems upon which en- diversity curves, life-form and proportions, and dangered species and threatened species depend may other compositional measures. Structural indicators in- be conserved’). clude many of the habitat variables measured in ecology Noss (1990) lists five categories of species that may and wildlife biology. Ideally, both biotic and habitat in- warrant special conservation effort, including intensive dicators should be measured at the community-eco- monitoring ( 1) ecological indicators: species that signal system and population-species levels of organization the effects of perturbations on a number of other spe- (Schamberger 1988). The functional indicators in Table cies with similar habitat requirements; (2) keystones: 1 include biotic variables from community ecology pivotal species upon which the diversity of a large part (e.g., predation rates) and biotic-abiotic variables from of a community depends; (3) umbrellas: species with (e.g., disturbance and nutrient cy- large area requirements, which if given sufficient pro-

Conservation Biology Volume 4, No. 4, December 1990 Noss Indicators for BiodiverSity 361 tected habitat area, will bring many other species under at the genetic level usually is restricted to zoo popula- protection; (4) flagships: popular, charismatic species tions of rare species, or species of commercial impor- that serve as symbols and rallying points for major con- tance such as certain trees. Lande and Barrowclough servation initiatives; and (5) vulnerables: species that ( 1987) discussed techniques available to directly mea- are rare, genetically impoverished, of low fecundity, de- sure and monitor genetic variation, and much of the pendent on patchy or unpredictable resources, ex- genetic portion of Table 1 is adapted from their paper. tremely variable in population density, persecuted, or Although some indices of morphological variability may otherwise prone to extinction in human-dominated be good indicators of genetic stress (Leary & Allendorf landscapes (see Terborgh & Winter 1980; Karr 1982; 1989), variation in morphology can be confounded by Soule 1983, 1987; Pimm et al. 1988; Simberloff 1988). phenotypic effects. Electrophoresis of tissue samples is Not all of these categories need to be monitored in any the preferred technique for monitoring heterozygosity given case. It may be that adequate attention to catego- and enzyme variability (allozymes), probably the most ries 2-5 would obviate the need to identlfy and monitor common measures of genetic variation. Heritability putative ecological indicator species (D. S. Wilcove, per- studies (e.g., offspring-parent regression, sib analysis) sonal communication). can be used to determine the level of genetic variation For species at risk, intensive monitoring may be di- for quantitative traits. Chromosomal polymorphisms rected at multiple population-level indicators, as well as can be monitored by karyotypic analysis, and the use of appropriate indicators at other levels - the genetic restriction endonucleases to cut DNA allows direct as- level, for example (Table 1). Measurements of morpho- sessment of genetic variation (Mlot 1989). The severity logical characters are often useful. The regression of of inbreeding depression can be evaluated from pedi- weight on size for and reptiles, for instance, grees (which, however, are seldom available for wild provides an index of the general health of a population populations). (Davis 1989). Within-individual morphological variabil- ity (e.g., fluctuating asymmetry in structures of bilater- ally symmetrical organisms) can be a sensitive indicator Implementation or environmental and genetic stress; composite indices that include information from several morphological Monitoring has not been a glamorous activity in science, characters are particularly useful (Leary & Allendorf in part because it has been perceived as blind data- 1989). Growth indicators (e.g., tree dbh) and reproduc- gathering (which, in some cases, it has been). The kinds tive output (e.g., number of fruits, germination rates) of questions that a scientist asks when initiating a re- are common monitoring targets for . search project - about causes and effects, probabilities, Often, monitoring at the population-species level is interactions, and alternative hypotheses - are not com- directed not at the population itself, but at habitat vari- monly asked by workers initiating a monitoring project. ables determined or assumed to be important to the In most agencies, monitoring and research projects are species. Habitat suitability indicators can be monitored uncoordinated and are carried out by separate branches. by a variety of techniques, including remote sensing of Explicit hypothesis-testingonly rarely has been a part of cover types required by a species (Cooperrider et al. monitoring studies, hence the insufficient concern for 1986). It has sometimes been assumed that monitoring experimental design and statistical analysis (Hinds habitat variables obviates the need to monitor popula- 1984). Perhaps monitoring will be most successful tions; however the presence of suitable habitat is no when it is perceived (and actually qualifies) as scientific guarantee that the species of interest is present. Popu- research and is designed to test specific hypotheses that lations may vary tremendously in density due to biotic are relevant to policy and management questions. In this factors, while habitat remains roughly context, monitoring is a necessary link in the “adaptive constant (Schamberger 1988). Conversely, inferences management” cycle that continuously refines regula- based solely on biotic variables such as population den- tions or management practices on the basis of data de- sity can be misleading. Among vertebrates, for example, rived from monitoring and analyzed with an emphasis concentrations of socially surbordinate individuals may on predicting impacts (Holling 1978). occur in areas of marginal habitat (Van Horne 1983). As an illustration of how a biodiversity monitoring Monitoring both habitat and population variables seems project might be implemented, imagine that a hypothet- to be essential in most cases. ical agency wants to assess status and trends in biolog- ical diversity in the Pacific Northwest. This grandiose project might be carried out in ten steps: Genetic 1. What and why? It is first necessary to establish In wild populations, demography is usually of more im- goals and objectives, and the “suknd points” of bio- mediate significance to population viability than is pop- diversity that the agency wishes to assess (and main- ulation genetics (Lande 1988). Due to cost, monitoring tain). This is more a matter of policy-making than of

Conservation Biology Volume 4, No. 4, December 1990 362 Indicators for Biodiversity Noss science. Goals for the Pacific Northwest might include: lands, for example, encompass a wide variety of silvicul- no net loss of forest cover or ; recovery of old- turd treatments. growth coniferous forests to twice the present acreage; 8.Design and implement a sampling scheme. Apply- recovery of native grasslands and shrub-steppe from ing principles of experimental design, select monitoring overgrazed condition; maintaining viable populations of sites for identified questions and objectives. A design all native species; and eradicating troublesome exotic might include intensive sampling of high-risk ecosys- species from federal lands. Sub-end points would cor- tems and species (identified in Step 4) and less intensive respond to these goals and encompass the health and sampling of general control and treatment areas identi- viability of all elements of biodiversity identified to be of fied in Step 7 (but with sampling points and plots se- concern. lected randomly within treatments). All treatments and 2. Gather and integrate existing data Existing bio- controls should be replicated. Randomized systematic diversity-relateddata bases in state natural heritage pro- sampling of the total regional landscape (stratified by grams, agency files, and from other sources would be ecosystem type, if desired) would provide background collected, digitized, and overlayed in a GIs. These data monitoring and may serve to identify unforeseen would be mapped for the region as a whole at a scale of stresses. Biology should drive the statistical design, how- 1:100,000 to 1:500,000 (see Scott et al. 1990). ever, rather than letting the design assume a life of its 3. Establish “baseline” conditions. From current own. data, determine the extent, distribution, and condition 9. Validate relationships between indicators and of existing ecosystem (vegetation) types and the prob- sub-endpoints Detailed, ongoing research is needed to able distribution of species of concern. Also, map the verlfy how well the selected indicators correspond to distribution and intensity of identified stressors (e.g., the biodiversity sub-end points of concern. For exam- tropospheric ozone, habitat fragmentation, road density, ple, does a particular fragmentation or edge index (such grazing intensity). as perimeter-arearatio or patch size frequency distribu- 4. Identtfy “hot spots” and ecosystems at high risk tion) really correspond to the intensity of abiotic and Proceeding from the previous two steps, delineate areas biotic edge effects or the disruption of dispersal be- of concentrated biodiversity (e.g., centers of species tween patches in the landscape? Does the relationship richness and endemism) and ecosystems and geograph- between indicator and sub-end point hold for the entire ical areas at high risk of impoverishment due to anthro- range of conditions encountered? pogenic stresses. Such areas warrant more intensive 10. Analyze trends and recommend management monitoring. In the Pacific Northwest, one prominent actions. Temporal series of measurements must be an- center of endemism is the Klamath-Siskiyou bioregion; alyzed in a statistically rigorous way and the results syn- an ecosystem type at high risk is old-growthforest (of all thesized into an assessment that is relevant to policy- species associations). makers. If the assessment can be translated into positive 5. Formulate specific questions to be answered by changes in planning assumptions, management direc- monitoring. These questions will be guided by the sub- tion and practices, laws and regulations, or environmen- end points, goals, and objectives identified in Step 1. tal policy, the monitoring project will have proved itself Questions might include: Is the ratio of native to exotic a powerful tool for conservation. range grasses increasing or decreasing? Is the average patch size of managed forests increasing or decreasing? Are populations of neotropical migrant birds stable?Are Acknowledgments listed endangered species recovering?It will help if pol- icy-makers can specrfy thresholds at which changes in Allen Cooperrider, Sandra Henderson, Bob Hughes, management practices or regulations will be imple- David Wilcove, and two anonymous referees provided mented. many helpful comments on an earlier draft of this manu- 6. Select indicators. Identrfy indicators of structural, script. functional, and compositional biodiversity at several lev- els of organization that correspond to identified sub- Literature Cited end points (Step 1) and questions (Step 5). Indicators can be chosen from the “laundry list” in Table 1, based Allen, T. F. H., and T. B. Starr. 1982. Hierarchy: perspectives for ecological complexity. University of Chicago Press, Chicago, on the criteria for ideal indicators reviewed above (un- Illinois. der “Why Indicators?”). 7. Zdentzyy control areas and treatments. For each Burgess, R. L., and D. M. Sharpe, editors. 1981. Forest island major ecosystem type, identrfy control areas (e.g., des- dynamics in man-dominatedlandscapes. Springer-Verlag, New ignated Wilderness and Research Natural Areas) and ar- York. eas subjected to different kinds and intensities of stress and management practices. Public and private forest Cairns, J. 1983. Are single species toxicity tests alone adequate

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