, Volume 14, Issue 1, pp 47–59 | Cite as

Direct Measurement Versus Surrogate Indicator Species for Evaluating Environmental Change and Biodiversity Loss

  • David B. LindenmayerEmail author
  • Gene E. Likens


The enormity and complexity of problems like environmental degradation and biodiversity loss have led to the development of indicator species and other surrogate approaches to track changes in environments and/or in biodiversity. Under these approaches particular species or groups of species are used as proxies for other biota, particular environmental conditions, or for environmental change. The indicator species approach contrasts with a direct measurement approach in which the focus is on a single entity or a highly targeted subset of entities in a given ecosystem but no surrogacy relationships with unmeasured entities are assumed. Here, we present a broad philosophical discussion of the indicator species and direct measurement approaches because their relative advantages and disadvantages are not well understood by many researchers, resource managers and policy makers. A goal of the direct measurement approach is to demonstrate a causal relationship between key attributes of the target ecosystem system (for example, particular environmental conditions) and the entities selected for measurement. The key steps in the approach are based on the fundamental scientific principles of hypothesis testing and associated direct measurement that drive research activities, management activities and monitoring programs. The direct measurement approach is based on four critical assumptions:(1) the ‘right’ entities to measure have been selected, (2) these entities are well known, (3) there is sufficient understanding about key ecological processes and (4) the entities selected can be accurately measured. The direct measurement approach is reductionist and many elements of the biota, many biotic processes and environmental factors must be ignored because of practical considerations. The steps in applying the indicator species approach are broadly similar to the direct measurement approach, except surrogacy relationships also must be quantified between a supposed indicator species or indicator group and the factors for which it is purported to be a proxy. Such quantification needs to occur via: (1) determining the taxonomic, spatial and temporal bounds for which a surrogacy relationship does and does not hold. That is, the extent of transferability of a given surrogate such as an indicator species to other biotic groups, to landscapes, ecosystems, environmental circumstances or over time in the same location can be determined; and (2) determining the ecological mechanisms underpinning a surrogacy relationship (for example, through fundamental studies of community structure). Very few studies have rigorously addressed these two tasks, despite the extremely widespread use of the indicator species approach and similar kinds of surrogate schemes in virtually all fields of environmental, resource and conservation management. We argue that this has the potential to create significant problems; thus, the use of an indicator species approach needs to be better justified. Attempts to quantify surrogacy relationships may reveal that, in some circumstances, the alternative of direct measurement of particular entities of environmental or conservation interest will be the best option.


environmental and biodiversity surrogates the indicator species approach direct ecological measurement ecological transferability environmental monitoring biodiversity conservation 



We thank M. Bailey, R. Muntz, P. Likens and C. Shepherd for their assistance in preparing this manuscript, including assistance in obtaining access to the very substantial literature on indicator species approaches. Valuable and provocative thoughts from a number of colleagues, referees and the editors considerably improved earlier versions of this manuscript.

Supplementary material

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Supplementary material 1 (DOC 75 kb)


  1. Australian Wildlife Conservancy. 2010. Measuring health of protected areas. Summer 2009/10. Perth: Australian Wildlife Conservancy.Google Scholar
  2. Billeter R, Liira J, Bailey D, Bugter R, Arens P, Augenstein I, Aviron S, Baudry J, Bukacek R, Burel F, Cerny M, De Glust G, De Cock R, Diekotter T, Dietz H, Dirksen J, Dormann C, Durka W, Frenzel M, Hamersky R, Hendrickx F, Herzog F, Klotz S, Koolstra B, Lausch A, Le Coeur D, Maelfait JP, Opdam P, Robalova M, Schermann A, Schermann N, Schmidt T, Schweiger O, Smulders MJ, Speelmans M, Simova P, Verboom J, van Wingerden WK, Zobel M, Edwards PJ. 2008. Indicators for biodiversity in agricultural landscapes: a pan-European study. J Appl Ecol 45:141–50.CrossRefGoogle Scholar
  3. Borghi M, Tognetti R, Monteforti G, Sebastiani L. 2008. Responses of two popular species (Populus alba and Populus x canadensis) to high copper concentrations. Environ Exp Bot 62:290–9.Google Scholar
  4. Braunisch V, Suchant R. 2008. Using ecological forest site mapping for long-term habitat suitability assessments in wildlife conservation–demonstrated for Capercaillie (Tetrao urogallus). For Ecol Manag 256:1209–21.CrossRefGoogle Scholar
  5. Cantarello E, Newton AC. 2008. Identifying cost-effective indicators to assess the conservation status of forested habitats in Natura 2000 sites. For Ecol Manag 256:815–26.CrossRefGoogle Scholar
  6. Charles DF, Binford MW, Furlong ET, Hites RA, Mitchell MJ, Norton SA, Oldfield F, Paterson MJ, Smol JP, Uutala AJ, White JR, Whitehead DR, Wise RJ. 1990. Paleoecological investigation of recent lake acidification in the Adirondack Mountains, N.Y. J Paleolimnol 3:195–241.Google Scholar
  7. Clarke M. 2008. Catering for the needs of fauna in fire management: science or just wishful thinking? Wildl Res 35:385–94.CrossRefGoogle Scholar
  8. Commonwealth of Australia. 2001. State of the environment report. Biodiversity. Canberra: Commonwealth of Australia.Google Scholar
  9. Cushman SA, McKelvey KS, Noon BR, McGarigal K. 2010. Use of abundance of one species as a surrogate for abundance of others. Conserv Biol 24:830–40.CrossRefPubMedGoogle Scholar
  10. Davis GE. 2005. National park environmental stewardship and “vital signs” monitoring: a case study from the Channel Islands National Park, California. Aquat Conserv 15:71–89.CrossRefGoogle Scholar
  11. de Moor FC, Ivanov VD. 2008. Global diversity of caddisflies (Trichoptera: Insecta) in freshwater. Hydrobiologica 595:393–407.CrossRefGoogle Scholar
  12. Dixit SS, Smol JP, Kingston JC, Charles DF. 1992. Diatoms-powerful indicators of environmental change. Environ Sci Technol 26:22–33.CrossRefGoogle Scholar
  13. Dooley JL, Bowers MA. 1998. Demographic responses to habitat fragmentation: experimental tests at the landscape and patch scale. Ecology 79:969–80.CrossRefGoogle Scholar
  14. Drever MC, Aitken KE, Norris AR, Martin K. 2008. Woodpeckers as reliable indicators of bird richness, forest health and harvest. Biol Conserv 141:624–34.CrossRefGoogle Scholar
  15. Dung NT, Webb EL. 2008. Combining local ecological knowledge and quantitative forest surveys to select indicator species for forest condition in central Viet Nam. Ecol Indic 8:767–70.Google Scholar
  16. Ellis CJ, Yahr R, Coppins BJ. 2009. Local extent of old-growth woodland modifies epiphyte response to climate change. J Biogeogr 36:302–13.CrossRefGoogle Scholar
  17. Elton CS. 1927. Animal ecology. London: Sidgwick and Jackson.Google Scholar
  18. Ernest SKM, Brown JH, Thibault KM, White EP, Goheen JR. 2008. Zero sum, the niche, and metacommunities: long-term dynamics of community assembly. Am Nat 172:E257–69.CrossRefPubMedGoogle Scholar
  19. Fox BJ. 1982. Fire and mammalian secondary succession in an Australian coastal heath. Ecology 63:1332–41.CrossRefGoogle Scholar
  20. Gegout J, Krizova E. 2003. Comparison of indicator values of forest understorey plant species in Western Carpathians (Slovakia) and Vosges Mountains (France). For Ecol Manag 182:1–11.CrossRefGoogle Scholar
  21. Halme P, Kptiaho JS, Ylisirno AL, Hottola J, Junninen K, Kouki J, Lindgren M, Mönkkönena M, Penttiläg R, Renvallh P, Siitonend J, Similäi M. 2009. Perennial polypores as indicators of annual and red-listed polypores. Ecol Indic 9:256–66.CrossRefGoogle Scholar
  22. Heino J. 2010. Are indicator groups and cross-taxon congruence useful for predicting biodiversity in aquatic ecosystems? Ecol Indic 10:112–17.CrossRefGoogle Scholar
  23. Hobbs RJ, Arico S, Aronson J, Baron JS, Bridgewater P, Cramer V, Epstein PR, Ewel JJ, Klink CA, Lugo AE, Nortone D, Ojima D, Richardson DM, Sanderson EW, Valladares F, Vilà M, Zamora R, Zobel M. 2006. Novel ecosystems: theoretical and management aspects of the new ecological world order. Glob Ecol Biogeogr 15:1–7.CrossRefGoogle Scholar
  24. Johnson EA, Miyanishi K. 2008. Testing the assumptions of chronosequences in succession. Ecol Lett 11:419–31.CrossRefPubMedGoogle Scholar
  25. Jung MP, Kim ST, Kim H, Lee JH. 2008. The biodiversity and community structure of ground-dwelling spiders in four different field margin types of agricultural landscapes in Korea. Appl Soil Ecol 38:185–95.CrossRefGoogle Scholar
  26. Kavanagh RP, Stanton MA. 2005. Vertebrate species assemblages and species sensitivity to logging in the forests of north-eastern New South Wales. For Ecol Manag 209:309–41.CrossRefGoogle Scholar
  27. Kirby MF, Smith AJ. 2006. Differential sensitivity of Flounder (Platichthys flesus) in response to oestrogenic chemical exposure: an issue for the design and interpretation of monitoring and research programmes. Mar Environ Res 62:315–25.CrossRefPubMedGoogle Scholar
  28. Klinka K, Krajina VJ, Ceska A, Scagel AM. 1989. Indicator plants of coastal British Columbia. Vancouver: UBC Press.Google Scholar
  29. Krebs C. 2008. The ecological world view. Melbourne: CSIRO Publishing.Google Scholar
  30. Kremen CA, Cameron A, Moilanen A, Phillips SJ, Thomas CD, Beentje H, Dransfield J, Fisher BL, Glaw F, Good TC, Harper GJ, Hijmans RJ, Lees DC, Louis E, Nussbaum RA, Raxworthy CJ, Razafimpahanana A, Schatz GE, Vences M, Vieites DR, Wright PC, Zjhra ML. 2008. Aligning conservation priorities across taxa in Madagascar with high-resolution planning tools. Science 320:222–6.CrossRefPubMedGoogle Scholar
  31. Landres PB, Verner J, Thomas JW. 1988. Ecological uses of vertebrate indicator species: a critique. Conserv Biol 2:316–28.CrossRefGoogle Scholar
  32. Lasne E, Bergerot B, Lek S, Laffaille P. 2008. Fish zonation and indicator species for the evaluation of the ecological status of rivers: examples of the Loire Basin (France). River Res Appl 23:877–90.CrossRefGoogle Scholar
  33. Leech TJ, Gormley AM, Seddon PJ. 2008. Estimating the minimum viable population size of Kaka (Nestor meridionalis) a potential surrogate species in New Zealand lowland forest. Biol Conserv 141:681–91.CrossRefGoogle Scholar
  34. Lehmkuhl JF, Peffer RD, O’Connell MA. 2008. Riparian and upland small mammals on the east slope of the Cascade Range, Washington. Northwest Sci 82:94–107.CrossRefGoogle Scholar
  35. Liira J, Schmidt T, Aavik T, Arens P, Augenstein I, Bailey D, Billeter R, Bukáček R, Burel F, De Blust G, De Cock R, Dirksen J, Edwards PJ, Hamerský R, Herzog F, Klotz S, Kiihn I, Le Coeur D, Miklová P, Roubalova M, Schweiger O, Smulders MJM, van Wingerden WKRE, Bugter R, Zobel M. 2008. Plant functional group composition and large-scale richness in European agricultural landscapes. J Veg Sci 19:3–14.CrossRefGoogle Scholar
  36. Lin KJ, Yo SP. 2008. The effect of organic pollution on the abundance and distribution of aquatic oligochaetes in an urban water basin, Taiwan. Hydrobiologica 596:213–23.CrossRefGoogle Scholar
  37. Lindenmayer DB. 2009a. Forest pattern and ecological process: a synthesis of 25 years of research. Melbourne: CSIRO Publishing.Google Scholar
  38. Lindenmayer DB. 2009b. Large-scale landscape experiments: lessons from Tumut. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  39. Lindenmayer DB, Cunningham RB. 1997. Patterns of co-occurrence among arboreal marsupials in the forests of central Victoria, southeastern Australia. Aust J Ecol 22:340–6.CrossRefGoogle Scholar
  40. Lindenmayer DB, Likens GE. 2009. Adaptive monitoring: a new paradigm for long-term research and monitoring. Trends Ecol Evol 24:482–6.CrossRefPubMedGoogle Scholar
  41. Lindenmayer DB, Likens GE. 2010. Effective ecological monitoring. Melbourne: CSIRO Publishing and Earthscan.Google Scholar
  42. Lindenmayer DB, Margules CR, Botkin DB. 2000. Indicators of biodiversity for ecologically sustainable forest management. Conserv Biol 14:941–50.CrossRefGoogle Scholar
  43. Lindenmayer DB, Wood JT, Cunningham RB, MacGregor C, Crane M, Michael D, Montague-Drake R, Brown D, Muntz R, Gill AM. 2008. Testing hypotheses associated with bird responses to wildfire. Ecol Appl 18:1967–83.CrossRefPubMedGoogle Scholar
  44. Lindenmayer DB, Wood J, Michael D, Crane M, MacGregor C, Montague-Drake R, McBurney L. 2009. Are gullies best for biodiversity? An empirical examination of Australian wet forest types. For Ecol Manag 258:169–77.CrossRefGoogle Scholar
  45. Luken JO. 1990. Directing ecological succession. New York: Chapman and Hall.Google Scholar
  46. Mace GM, Baillie JE. 2007. The 2010 biodiversity indicators: challenges for science and policy. Conserv Biol 21:1406–13.CrossRefPubMedGoogle Scholar
  47. MacSwiney MC, Clarke FM, Racey PA. 2008. What you see is not what you get: the role of ultrasonic detectors in increasing inventory completeness in Neotropical bat assemblages. J Appl Ecol 45:1364–71.CrossRefGoogle Scholar
  48. Maher W, Norris RH. 1990. Water quality assessment programs in Australia: deciding what to measure and how and where to use bioindicators. Environ Monit Assess 14:115–30.CrossRefGoogle Scholar
  49. Mariogomez I, Soto M. 2006. Cell and tissue markers in mussel, histopathology in hake and anchovy from Bay of Biscay after Prestige Oil spill (monitoring campaign 2003. Mar Pollut Bull 53:287–304.CrossRefGoogle Scholar
  50. McMullan-Fischer SJ, Kirkpatrick JB, May TW, Pharo EJ. 2010. Surrogates for macrofungi and mosses in reservation planning. Conserv Biol 24:730–6.CrossRefGoogle Scholar
  51. Milledge DR, Palmer CL, Nelson JL. 1991. ‘Barometers of change’: the distribution of large owls and gliders in Mountain Ash forests of the Victorian Central Highlands and their potential as management indicators. Lunney D, editor. Conservation of Australia’s forest fauna. Sydney: Royal Zoological Society of NSW. pp 53–65.Google Scholar
  52. Morrison ML, Marcot BG, Mannan RW. 2006. Wildlife-habitat relationships. Concepts and applications. Washington, DC: Island Press.Google Scholar
  53. Niemi GJ, McDonald ME. 2004. Application of ecological indicators. Annu Rev Ecol Evol Syst 35:89–111.CrossRefGoogle Scholar
  54. Oster M, Persson K, Eriksson O. 2008. Validation of plant diversity indicators in semi-natural grasslands. Agric Ecosyst Environ 125:65–72.CrossRefGoogle Scholar
  55. Parmesan C. 2006. Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–69.CrossRefGoogle Scholar
  56. Patthey P, Wirthner S, Signorell N, Arlettaz R. 2008. Impact of outdoor winter sports on the abundance of a key indicator species of alpine ecosystems. J Appl Ecol 45:1704–11.CrossRefGoogle Scholar
  57. Pearce J, Venier L. 2005. Small mammals as bioindicators of sustainable forest management. For Ecol Manag 208:153–75.CrossRefGoogle Scholar
  58. Potapova M, Charles DF. 2007. Diatom metrics for monitoring eutrophication in rivers of the United States. Ecol Indic 7:48–70.CrossRefGoogle Scholar
  59. Price SJ, Howe RW, Hanowski JM, Regal RR, Niemi GJ, Smith CR. 2007. Are anurans of Great Lakes coastal wetlands reliable indicators of ecological condition? J Great Lakes Res 33:211–23.CrossRefGoogle Scholar
  60. Proctor J, Woodell RJ. 1975. The ecology of ultramafic soils. Adv Ecol Res 9:255–366.CrossRefGoogle Scholar
  61. Reader R. 1988. Using the guild concept in the assessment of tree harvesting effect on understorey herbs: a cautionary note. Environ Manage 12:803–8.CrossRefGoogle Scholar
  62. Reading CJ, Luiselli LM, Akani GC, Bonnet X, Amori G, Ballouard JM, Filippi E, Naulleau G, Pearson D, Rugiero L. 2010. Are snake populations in widespread decline? Biol Lett. doi: 10.1098/rsbl.2010.0373.
  63. Reid PC, Edwards M, Johns DG. 2008. Trans-arctic invasion in modern times. Science 322:528–9.CrossRefPubMedGoogle Scholar
  64. Rodrigues ASL, Brooks TM. 2007. Shortcuts for biodiversity conservation planning: the effectiveness of surrogates. Annu Rev Ecol Evol Syst 38:713–37.CrossRefGoogle Scholar
  65. Roth T, Weber D. 2008. Top predators as indicators for species richness? Prey species are just as useful. J Appl Ecol 45:987–1011.CrossRefGoogle Scholar
  66. Seddon PJ, Leech T. 2008. Conservation short cut, or long and winding road? A critique of umbrella species criteria. Oryx 42:240–5.CrossRefGoogle Scholar
  67. Sergio F, Newton I, Marchesi L. 2008. Top predators: much debate, few data. J Appl Ecol 45:992–9.CrossRefGoogle Scholar
  68. Sodhi NS, Liow L-H, Bazzazz F. 2004. Avian extinctions from tropical and subtropical forests. Annu Rev Ecol Evol Syst 35:323–45.CrossRefGoogle Scholar
  69. Spencer J. 1991. Indications of antiquity: some observations on the nature of plants associated with ancient woodland. Br Wildl 2:90–102.Google Scholar
  70. Steffen W, Burbidge A, Hughes L, Kitching R, Lindenmayer DB, Musgrave W, Stafford-Smith M, Werner PA. 2009. Australia’s biodiversity and climate change. Melbourne: CSIRO Publishing.Google Scholar
  71. Strayer DL, Dudgeon D. 2010. Freshwater biodiversity conservation: recent progress and future challenges. J North Am Benthol Soc 29:344–58.Google Scholar
  72. The Heinz Center. 2008. The state of the nation’s ecosystems 2008. Washington, DC: The H. John Heinz III Centre for Science, Economics and the Environment and Island Press.Google Scholar
  73. Thompson SA, Thompson GG. 2008. Rehabilitation index for evaluating restoration of terrestrial ecosystems using the reptile assemblage as the bio-indicator. Ecol Indic 8:530–49.CrossRefGoogle Scholar
  74. Torres MA, Barros MP, Campos SC, Pinto E, Rajamani S, Sayre RT, Colepicolo P. 2008. Biochemical biomarkers in algae and marine pollution: a review. Exotoxicol Environ Saf 71:1–15.CrossRefGoogle Scholar
  75. Vié J-C, Hilton-Taylor C, Stuart SN. 2009. Wildlife in a changing world. An analysis of the 2008 IUCN red list of threatened species. Gland: IUCN.Google Scholar
  76. Wake DB, Vredenburg VT. 2008. Are we in the midst of the sixth mass extinction? View from the world of amphibians. Proc Natl Acad Sci 105:11466–73.CrossRefPubMedGoogle Scholar
  77. Wakelin J, Hill TR. 2007. The impact of land transformation on breeding Blue Swallows Hirundo atrocaerulea Sundevall, in Kwazulu-Natal, South Africa. J Nat Conserv 15:245–55.CrossRefGoogle Scholar
  78. Walker KF. 1981. Ecology of freshwater mussels in the River Murray. Australian Water Resources Council Technical Paper No. 63. Canberra: Australian Government Publishing Service.Google Scholar
  79. Walpole M, Almond RE, Besancon C, Butchart SH, Campbell-Lendrum D, Carr GM, Collen B, Collette L, Davidson NC, Dulloo E, Fazel AM, Galloway JN, Gill M, Goverse T, Hockings M, Leaman DJ, Morgan DH, Revenga C, Rickwood CJ, Schutyser F, Simons S, Statterfield AJ, Tyrell TD, Vie J-C, Zimsky M. 2009. Tracking progress toward the 2010 biodiversity target and beyond. Science 325:1503–4.CrossRefPubMedGoogle Scholar
  80. Whitfield-Gibbons J, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT. 2000. The global decline of reptiles, deja vu amphibians. Bioscience 50:653–66.CrossRefGoogle Scholar
  81. Woodward A, Jenkins K, Schreiner EG. 1999. The role of ecological theory in long-term monitoring: report on a workshop. Nat Areas J 19:223–33.Google Scholar
  82. Wright-Stow AE, Winterbourn MJ. 2003. How well do New Zealand’s stream-monitoring indicators, the Macroinvertebrate Community Index and its quantitative variant, correspond? N Z J Mar Freshw Res 37:461–70.CrossRefGoogle Scholar
  83. Zamora J, Verdu JR, Galante E. 2007. Species richness in Mediterranean agroecosystems: spatial and temporal analysis for biodiversity conservation. Biol Conserv 134:113–21.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Fenner School of Environment and SocietyThe Australian National UniversityCanberraAustralia
  2. 2.Cary Institute of Ecosystem StudiesMillbrookUSA

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