Abstract
Surrogate species approaches, including flagship, focal, keystone, indicator, and umbrella, are considered an effective means of conservation planning. For conservation biologists to apply surrogates with confidence, they must have some idea of the effectiveness of surrogates for the circumstances in which they will be applied. We reviewed tests of the effectiveness of surrogate species planning to see if research supports the development of generalized rules for (1) determining when and where surrogate species are an effective conservation tool and (2) how surrogate species should be selected such that the resulting conservation plan will effectively protect biodiversity or achieve other conservation goals. The context and methods of published studies were so diverse that we could not draw general conclusions about the spatial or temporal scales, or ecosystems or taxonomic groups for which surrogate species approaches will succeed. The science of surrogate species can progress by (1) establishing methods to compare diverse measures of effectiveness; (2) taking advantage of data-rich regions to examine the potential effectiveness of surrogate approaches; (3) incorporating spatial scale as an explanatory variable; (4) evaluating surrogate species approaches at broader temporal scales; (5) seeking patterns that will lead to hypothesis driven research; and (6) monitoring surrogate species and their target species.
Similar content being viewed by others
References
Andelman S.J. and Fagan W.F. (2000). Umbrellas and flagships: efficient conservation surrogates or expensive mistakes?. Proc. Natl. Acad. Sci. USA 97: 5954–5959
Arnqvist G. and Wooster D. (1995). Meta-analysis: synthesizing research findings in ecology and evolution. Trends Ecol. Evol. 10: 236–240
Baldi A. (2003). Using higher taxa as surrogates of species richness: a study based on 3700 Coleoptera, Dipteraand Acari species in Central-Hungarian reserves. Basic Appl. Ecol. 4: 589–593
Belovsky G.E., Botkin D.B., Crowl T.A., Cummins K.W., Franklin J.F., Hunter M.L., Joern A., Lindenmayer D.B., MacMahon J.A., Margules C.R. and Scott J.M. (2004). Ten suggestions to strengthen the science of ecology. Bioscience 54: 345–351
Berger J. (1997). Population constraints associated with the use of black rhino as an umbrella species for desert herbivores. Conserv. Biol. 11: 69–78
Bond W. (2001). Keystone species – hunting the snark?. Science 292: 63–64
Bonn A., Rodrigues A.S.L. and Gaston K.J. (2002). Threatened and endemic species: are they good indicators of patterns of biodiversity on a national scale?. Ecol. Lett. 5: 733–741
Brooker L. (2002). The application of focal species knowledge to landscape design in agricultural lands using the ecological neighbourhood as a template. Landscape Urban Plan. 60: 185–210
Brooks T.M., Rodrigues A.S.L. and Fonseca G.A.B. (2004). Protected areas and species. Conserv. Biol. 18: 616–618
Bushman B.J. (1994). Vote-counting procedures in meta-analysis. In: Cooper, H. and Hedges, L.V. (eds) The Handbook of Research Synthesis, pp 193–214. Russell Sage Foundation, NY
Cardoso P., Silva I., Serrano A.R.M. and Oliveira N.G. (2004). Higher taxa surrogates of spider (Araneae) diversity and their efficiency in conservation. Biol. Conserv. 117: 453–459
Caro T., Engilis A., Fitzherbert E. and Gardner T. (2004). Preliminary assessment of the flagship species concept at a small scale. Anim. Conserv. 7: 63–70
Caro T.M. (2001). Species richness and abundance of small mammals inside and outside an African national park. Biol. Conserv. 98: 251–257
Caro T.M. (2003). Umbrella species: critique and lessons from East Africa. Anim. Conserv. 86: 171–181
Caro T.M. and O’Doherty G. (1999). On the use of surrogate species in conservation biology. Conserv. Biol. 13: 805–814
Carroll C., Noss R.E., Paquet P.C. and Schumaker N.H. (2003). Use of population viability analysis and reserve selection algorithms in regional conservation plans. Ecol. Appl. 13: 1773–1789
Chase M.K., Kristan W.B., Lynam A.J., Price M.V. and Rotenberry J.T. (2000). Single species as indicators of species richness and composition in California coastal sage scrub birds and small mammals. Conserv. Biol. 14: 474–487
Coulson T., Mace G.M., Hudson E. and Possingham H. (2001). The use and abuse of population viability analysis. Trends Ecol. Evol. 16: 219–221
Dietz J.M., Dietz L.A. and Nagagata E.Y. (1994). The effective use of flagship species for conservation of biodiversity: the example of lion tamarins in Brazil. In: Olney, P.J.S., Mace, G.M., and Feistner, A.T.C. (eds) Creative Conservation: Interactive Management of Wild and Captive Animals, pp 32–49. Chapman and Hall, London
Fernandez-Duque E. and Valeggia C. (1994). Meta-analysis: a valuable tool in conservation research. Conserv. Biol. 8: 555–561
Fjeldsa J. (2000). The relevance of systematics in choosing priority areas for global conservation. Environ. Conserv. 27: 67–75
Flather C.H., Wilson K.R., Dean D.J. and McComb W.C. (1997). Identifying gaps in conservation networks: of indicators and uncertainty in geographic-based analyses. Ecol. Appl. 7: 531–542
Fleishman E., Betrus C.J. and Blair R.B. (2003). Effects of spatial scale and taxonomic group on partitioning of butterfly and bird diversity in the Great Basin, USA. Landscape Ecol. 18: 675–685
Fleishman E., Betrus C.J., Blair R.B., MacNally R. and Murphy D.D. (2002). Nestedness analysis and conservation planning: the importance of place, environment, and life history across taxonomic groups. Oecologia 133: 78–89
Fleishman E., Blair R.B. and Murphy D.D. (2001). Empirical validation of a method for umbrella species selection. Ecol. Appl. 11: 1489–1501
Fleishman E. and Mac Nally R. (2002). Topographic determinants of faunal nestedness in Great Basin butterfly assemblages: Applications to conservation planning. Conserv. Biol. 16: 422–429
Fleishman E., Murphy D.D. and Brussard P.E. (2000). A new method for selection of umbrella species for conservation planning. Ecol. Appl. 10: 569–579
Garson J., Aggarwal A. and Sarkar S. (2002). Birds as surrogates for biodiversity: an analysis of a data set from southern Quebec. J. Biosci. 27: 347–360
Gates S. (2002). Review of methodology of quantitative reviews using meta-analysis in ecology. J. Anim. Ecol. 71: 547–557
Hess G.R., Koch F., Rubino M., Eschalbach K., Drew A. and Favreau J. 2004. Comparing potential effectiveness of conservation planning approaches in central North Carolina USA. Biological Conservation (in press).
Hughes J.B., Daily G.C. and Ehrlich P.R. (2000). Conservation of insect diversity: a habitat approach. Conserv. Biol. 14: 1788–1797
Hurlbert S.H. (1997). Functional importance vs keystoneness: reformulating some questions in theoretical biocenology. Aust. J. Ecol. 22: 369–382
ISI 2004. ISI Web of Science. Version 1.2. Accessed June 2004, www.isiwebofknowledge.com.
Jansson G. (1998). Guild indicator species on a landscape scale – an example with four avian habitat specialists. Ornis Fennica 75: 119–127
Kati V., Devillers P., Dufrene M., Legakis A., Vokou D. and Lebrun P. (2004). Testing the value of six taxonomic groups as biodiversity indicators at a local scale. Conserv. Biol. 18: 667–675
Kerr J.T., Sugar A. and Packer L. (2000). Indicator taxarapid biodiversity assessmentand nestedness in an endangered ecosystem. Conserv. Biol. 14: 1726–1734
Kremen C. (1992). Assessing the indicator properties of species assemblages for natural areas monitoring. Ecol. Appl. 2: 203–217
Lambeck R.J. (1997). Focal species: a multi-species umbrella for nature conservation. Conserv. Biol. 11: 849–856
Lambeck R.J. (2002). Focal species and restoration ecology: response to Lindenmayer et al. Conserv. Biol. 16: 549–551
Landres P.B., Verner J. and Thomas J.W. (1988). Ecological uses of vertebrate indicator species – a critique. Conserv. Biol. 2: 316–328
Launer A.E. and Murphy D.D. (1994). Umbrella species and the conservation of habitat fragments: a case of a threatened butterfly and a vanishing grassland ecosystem. Biol. Conserv. 69: 145–153
Lawler J.J., White D., Sifneos J.C. and Master L.L. (2003). Rare species and the use of indicator groups for conservation planning. Conserv. Biol. 17: 875–882
Leader-Williams N. and Dublin H.T. (2000). Charismatic megafauna as ‘flagship species’. In: Entwistle, A. and Dunstone, N. (eds) Priorities for the Conservation of Mammalian Diversity: Has the Panda had its day?, pp 53–81. Cambridge University Press, Cambridge, UK
Lindenmayer D.B., Cunningham R.B., Donnelly C.F. and Lesslie R. (2002a). On the use of landscape surrogates as ecological indicators in fragmented forests. Forest Ecol. Manage. 159: 203–216
Lindenmayer D.B. and Lacy R.C. (2002). Small mammals, habitat patches and PVA models: a field test of model predictive ability. Biol. Conserv. 103: 247–265
Lindenmayer D.B., Manning A.D., Smith P.L., Possingham H.P., Fischer J., Oliver I. and McCarthy M.A. (2002b). The focal-species approach and landscape restoration: a critique. Conserv. Biol. 16: 338–345
Linnell J.D.C., Swenson J.E. and Andersen R. (2000). Conservation of biodiversity in Scandinavian boreal forests: large carnivores as flagships, umbrellas, indicators, or keystones?. Biodivers. Conserv. 9: 857–868
LTER. 2003. US long term ecological research network. Accessed 28 July 2004. http://lternet.edu.r.
Lund M.P. and Rahbek C. (2002). Cross-taxon congruence in complementarity and conservation of temperate biodiversity. Anim. Conserv. 5: 163–171
Mac Nally R. and Fleishman E. (2002). Using “indicator” species to model species richness: Model development and predictions. Ecol. Appl. 12: 79–92
Mac Nally R. and Fleishman E. (2004). A successful predictive model of species richness based on indicator species. Conserv. Biol. 18: 646–654
Manne L.L. and Williams P.H. (2003). Building indicator groups based on species characteristics can improve conservation planning. Anim. Conserv. 6: 291–297
Margules C.R. and Austin M.P. (1994). Biological models for monitoring species decline: the construction and use of databases. Phil. Transact. Biol. Sci. 344: 69–75
Margules C.R. and Pressey R.L. (2000). Systematic conservation planning. Nature 405: 243–253
Mikusinski G., Gromadzki M. and Chylarecki P. (2001). Woodpeckers as indicators of forest bird diversity. Conserv. Biol. 15: 208–217
Mills L.S., Soule M.E. and Doak D.F. (1993). The keystone-species concept in ecology and conservation. Bioscience 43: 219–224
Mittermeier R.A. (1988). Primate diversity and the tropical forest: case studies from Brazil and Madagascar and the importance of the megadiversity countries. In: Wilson, E.O. (eds) Biodiversity, pp 145–154. National Academy Press, Washington, DC
Moore J.L., Balrnford A., Brooks T., Burgess N.D., Hansen L.A., Rahbek C. and Williams P.H. (2003). Performance of sub-Saharan vertebrates as indicator groups for identifying priority areas for conservation. Conserv. Biol. 17: 207–218
Moore N.W. (1962). The heaths of Dorset and their conservation. J. Ecol. 50: 369–391
Moritz C., Richardson K.S., Ferrier S., Monteith G.B., Stanisic J., Williams S.E. and Whiffin T. (2001). Biogeographical concordance and efficiency of taxon indicators for establishing conservation priority in a tropical rainforest biota. Proc. Roy. Soc. Lond. Ser. B-Biol. Sci. 268: 1875–1881
NatureServe. 2003. A Network Connecting Science with Conservation. Accessed 7 May 2003, http://www.natureserve.org.
Negi H.R. and Gadgil M. (2002). Cross-taxon surrogacy of biodiversity in the Indian Garhwal Himalaya. Biol. Conserv. 105: 143–155
Niemi G.J., Hanowski J.M., Lima A.R., Nicholls T. and Weiland N. (1997). A critical analysis on the use of indicator species in management. J. Wildlife Manage. 61: 1240–1252
Noon B.R., Murphy D.D., Beissinger S.R., Shaffer M.L. and Dellasala D. (2003). Conservation planning for US National Forests: Conducting comprehensive biodiversity assessments. Bioscience 53: 1217–1220
Noss R.F., Carroll C., Vance-Borland K. and Wuerthner G. (2002). A multicriteria assessment of the irreplaceability and vulnerability of sites in the Greater Yellowstone Ecosystem. Conserv. Biol. 16: 895–908
Noss R.F., Quigley H.B., Hornocker M.G., Merrill T. and Paquet P.C. (1996). Conservation biology and carnivore conservation in the Rocky Mountains. Conserv. Biol. 10: 949–963
Oliver I. and Beattie A.J. (1996). Invertebrate morphospecies as surrogates for species: A case study. Conserv. Biol. 10: 99–109
Paine R.T. (1969). A note on trophic complexity and community stability. Am. Nat. 103: 91–93
Pearson D.L. and Carroll S.S. (1999). The influence of spatial scale on cross-taxon congruence patterns and prediction accuracy of species richness. J. Biogeogr. 26: 1079–1090
Poiani K.A., Merrill M.D. and Chapman K.A. (2001). Identifying conservation-priority areas in a fragmented Minnesota landscape based on the umbrella species concept and selection of large patches of natural vegetation. Conserv. Biol. 15: 513–522
Power M.E., Tilman D., Estes J.A., Menge B.A., Bond W.J., Mills L.S., Daily G., Castilla J.C., Lubchenko J. and Paine R.T. (1996). Challenges in the quest for keystones. Bioscience 46: 609–620
Prendergast J.R., Quinn R.M., Lawton J.H., Eversham B.C. and Gibbons D.W. (1993). Rare species, the coincidence of diversity hotspots and conservation strategies. Nature 365: 335–337
Pressey R.L. and Nicholls A.O. (1989). Efficiency in conservation evaluation: scoring versus iterative approaches. Biol. Conserv. 50: 199–218
Pullin A.S., Knight T.M., Stone D.A. and Charman K. (2004). Do conservation managers use scientific evidence to support their decision-making?. Biol. Conserv. 119: 245–252
Ranius T. (2002). Biodivers. Conserv. 11: 931–941
Reyers B., Kruger M. and Jaarsveld A.S. (2000). Complementarity as a biodiversity indicator strategy. Proc. Roy. Soc. Lond. Ser. B-Biol. Sci. 267: 505–513
Ricketts T.H., Daily G.C. and Ehrlich P.R. (2002). Does butterfly diversity predict moth diversity? Testing a popular indicator taxon at local scales. Biol. Conserv. 103: 361–370
Ricketts T.H., Dinerstein E., Olson D.M. and Loucks C. (1999). Who's where in North America?. Bioscience 49: 369–381
Roberge J.M. and Angelstam P. (2004). Usefulness of the umbrella species concept as a conservation tool. Conserv. Biol. 18: 76–85
Rubino M.J. and Hess G.R. (2003). Planning open spaces for wildlife II: mapping and verifying focal species habitat. Landscape Urban Plan. 64: 89–104
Rubinoff D. (2001). Evaluating the California gnatcatcher as an umbrella species for conservation of southern California coastal sage scrub. Conserv. Biol. 15: 1374–1383
Ryti R.T. (1992). Effect of the focal taxon on the selection of nature reserves. Ecol. Appl. 2: 404–410
Sahlen G. and Ekestubbe K. (2001). Identification of dragonflies (Odonata) as indicators of general species richness in boreal forest lakes. Biodivers. Conserv. 10: 673–690
Sauberer N., Zulka K.P., Abensperg-Traun M., Berg H.M., Bieringer G., Milasowszky N., Moser D., Plutzar C., Pollheimer M., Storch C., Trostl R., Zechmeister H. and Grabherr G. (2004). Surrogate taxa for biodiversity in agricultural landscapes of eastern Austria. Biol. Conserv. 117: 181–190
Sauer J.R., Hines J.E. and Fallon J. 2002. The North American Breeding Bird Survey, results and analysis 1966 – 2001. Version 2002.1. USGS Patuxent Wildlife Research CenterLaurel, MD.
Simberloff D. (1980). A succession of paradigms in ecology: essentialism to materialism and probabilism. Synthese 43: 3–39
Simberloff D. (1998). Flagships, umbrellas and keystones: is single-species management passe in the landscape era?. Biol. Conserv. 83: 247–257
Su J.C., Debinski D.M., Jakubauskas M.E. and Kindscher K. (2004). Beyond species richness: community similarity as a measure of cross-taxon congruence for coarse-filter conservation. Conserv. Biol. 18: 167–173
Summerville K.S., Ritter L.M. and Crist T.O. (2004). Forest moth taxa as indicators of lepidopteran richness and habitat disturbance: a preliminary assessment. Biol. Conserv. 116: 9–18
Suter W., Graf R.F. and Hess R. (2002). Capercaillie (Tetrao urogallus)avian biodiversity: testing the umbrella-species concept. Conserv. Biol. 16: 778–788
Swengel S.R. and Swengel A.B. (1999). Correlations in abundance of grassland songbirds and prairie butterflies. Biol. Conserv. 90: 1–11
UNEP 2002. World Conservation monitoring centre – conservation databases. Access date: 28 July 2004. http://www.wcmc.org/uk/cis.
Schotman A., Claassen F., Sparenburg G. and Langevelde F. (2000). Competing land use in the reserve site selection problem. Landscape Ecol. 15: 243–256
Warman L.D., Forsyth D.M., Sinclair A.R.E., Freemark K., Moore H.D., Barrett T.W., Pressey R.L. and White D. (2004). Species distributions, surrogacy, and important conservation regions in Canada. Ecol. Lett. 7: 374–379
Wilcox B.A. 1984. In situ conservation of genetic resources: determinants of minimum area requirements. In: McNeely J.A. and Miller K.R. (eds), National Parks, Conservation, and Development: The Role of Protected Areas in Sustaining Society. Smithsonian Institution Press, Washington, D.C., pp. 825.
Williams P.H., Burgess N.D. and Rahbek C. (2000). Flagship species, ecological complementarity and conserving the diversity of mammals and birds in sub-Saharan Africa. Anim. Conserv. 3: 249–260
ZMUC (Zoological Museum University of Copenhagen) 2004. A continent-wide blueprint for conservation action in Africa: description of the databases. Accessed: 20 July 2004, http://www.zmuc.dk/commonweb/research/biodata.htm.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Favreau, J.M., Drew, C.A., Hess, G.R. et al. Recommendations for Assessing the Effectiveness of Surrogate Species Approaches. Biodivers Conserv 15, 3949–3969 (2006). https://doi.org/10.1007/s10531-005-2631-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-005-2631-1