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Promising yet variable performance of cross-taxon biodiversity surrogates: a test in two marine habitats at multiple times

Biodiversity and Conservation volume 29, pages 3067–3089 (2020)Cite this article

Abstract

Surrogates are a potential solution to the often-cited problem of there being insufficient information for biodiversity assessments or conservation planning. Cross-taxon surrogacy is the ability of a group of well-known taxa to represent variation in other poorly known taxa. To date, tests of the effectiveness of cross-taxon surrogacy in marine environments have yielded variable results and a significant qualification to the outcomes of tests that have demonstrated surrogacy is the near absence of tests for its persistence through time. This study tested for cross-taxon surrogacy and its persistence through time for three surrogates (crustaceans, molluscs, polychaetes). We used data on biodiversity variables and species assemblages of the surrogates and their targets that had been collected during multiple sampling events over 2.5 years in two habitats (seagrass, unvegetated sediment) in a large bay in south-eastern Australia. We tested surrogacy by fitting a series of linear models using generalized least squares for biodiversity variables and by Mantel tests of dissimilarity matrices of species assemblages. We also tested whether the type of data transformation affected Mantel tests. We found that each of the groups were effective surrogates for some but not all biodiversity variables (with molluscs or polychaetes being effective surrogates for species richness in both habitats), that none of the groups were effective surrogates for species assemblages, and that the outcomes of Mantel tests of dissimilarity matrices of surrogates and their targets were unaffected by the data transformation used. We conclude that while our results for surrogacy for biodiversity variables are promising the inconsistent results from other studies argues for caution about their application beyond the area and context in which they were assessed. The lack of evidence that we found for surrogates of species assemblages, and similar lack of evidence from other studies, suggests that assemblage-level surrogates are unlikely to be useful in biodiversity surveys.

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References

  • Allen AP, Whittier TR, Larsen DP, Kaufmann PR, O'Connor RJ, Hughes RM, Stemberger RS, Dixit SS, Brinkhurst RO, Herlihy AT, Paulsen SG (1999) Concordance of taxonomic composition patterns across multiple lake assemblages: effects of scale, body size, and land use. Can J Fish Aq Sci 56:2029–2040

    Google Scholar 

  • Anderson MJ, Connell SD, Gillanders BM, Diebel CE, Blom WM, Saunders JE, Landers TJ (2005) Relationships between taxonomic resolution and spatial scales of multivariate variation. J Anim Ecol 74:636–646

    Google Scholar 

  • Beesley PL, Ross GJB, Glasby CJ (eds) (2000) Polychaetes & allies: the southern synthesis. Fauna of Australia. Vol. 4A Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula. CSIRO Publishing, Melbourne

  • Beger M, Jones GP, Munday PL (2003) Conservation of coral reef biodiversity: a comparison of reserve selection procedures for corals and fishes. Biol Conserv 111:53–62

    Google Scholar 

  • Bell JD, Steffe AS, Westoby M (1988) Location of seagrass beds in estuaries: effects on associated fish and decapods. J Exp Mar Biol Ecol 122:127–146

    Google Scholar 

  • Brusca RC, Lindberg DR, Ponder WF (2016) Phylum Mollusca. In: Brusca RC, Moore W, Shuster SM (eds) Invertebrates. Sinauer Associates, Sunderland, pp 453–530

    Google Scholar 

  • Clark GF, Kelaher BP, Dafforn KA, Coleman MA, Knott NA, Marzinelli EM, Johnston EL (2015) What does impacted look like? High diversity and abundance of epibiota in modified estuaries. Environ Pollut 196:12–20

    CAS  PubMed  Google Scholar 

  • Clarke KR, Gorley RN (2015) PRIMER v7: User manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Corte GN, Checon HH, Fonseca G, Vieira DC, Gallucci F, Di Domenico M, Amaral ACZ (2017) Cross-taxon congruence in benthic communities: searching for surrogates in marine sediments. Ecol Indic 78:173–182

    Google Scholar 

  • Crawley MJ (2009) The R book, 2nd edn. Wiley, Chichester

    Google Scholar 

  • Crossman S, Li O (2015) Surface hydrology polygons (regional). Geoscience Australia, Canberra

    Google Scholar 

  • CSIRO (1993) Jervis Bay Marine Ecological Studies Final Report. CSIRO Division of Fisheries, Jervis Bay

  • Duarte CM (1989) Temporal biomass variability and production/biomass relationships of seagrass communities. Mar Ecol Progr Series 51:269–276

    Google Scholar 

  • Edgar GJ, Barrett NS (2002) Benthic macrofauna in Tasmanian estuaries: scales of distribution and relationships with environmental variables. J Exp Mar Biol Ecol 270:1–24

    Google Scholar 

  • Eglington SM, Noble DG, Fuller RJ (2012) A meta-analysis of spatial relationships in species richness across taxa: Birds as indicators of wider biodiversity in temperate regions. J Nat Conserv 20:301–309

    Google Scholar 

  • Fisher R, Knowlton N, Brainard RE, Caley MJ (2011) Differences among major taxa in the extent of ecological knowledge across four major ecosystems. PLoS ONE 6:e26556

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gaston KJ, Williams PH (1996) Spatial patterns in taxonomic diversity. In: Gaston KJ (ed) Biodiversity. A biology of numbers and difference, Blackwell Science, Oxford, pp 202–229

    Google Scholar 

  • Gladstone W (2002) The potential value of indicator groups in the selection of marine reserves. Biol Conserv 104:211–220

    Google Scholar 

  • Gladstone W, Owen V (2005) The potential value of surrogates for the selection and design of marine reserves for biodiversity and fisheries. In: Day JC, Senior J, Monk S, Neal W (eds) First international marine protected areas congress, 23–27 October 2005, conference proceedings (IMPAC1, Geelong), pp 224–226

  • Grantham HS, Pressey RL, Wells JA, Beattie AJ (2010) Effectiveness of biodiversity surrogates for conservation planning: different measures of effectiveness generate a kaleidoscope of variation. PLoS ONE 5:e11430

    PubMed  PubMed Central  Google Scholar 

  • Heino J (2010) Are indicator groups and cross-taxon congruence useful for predicting biodiversity in aquatic ecosystems? Ecol Indic 10:112–117

    Google Scholar 

  • Hess GR, Bartel RA, Leidner AK, Rosenfeld KM, Rubino MJ, Snider SB, Ricketts TH (2006) Effectiveness of biodiversity indicators varies with extent, grain, and region. Biol Conserv 132:448–457

    Google Scholar 

  • Hirst AJ (2008) Surrogate measures for assessing cryptic faunal biodiversity on macroalgal-dominated subtidal reefs. Biol Conserv 141:211–220

    Google Scholar 

  • Hughes TP, Bellwood DR, Connolly SR (2002) Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs. Ecol Lett 5:775–784

    Google Scholar 

  • Hutchings P (1998) Biodiversity and functioning of polychaetes in benthic sediments. Biodivers Conserv 7:1133–1145

    Google Scholar 

  • Hutchings PA, Jacoby C (1994) Temporal and spatial patterns in the distribution of infaunal polychaetes in Jervis Bay, New South Wales. Memoir Natl Hist 162:441–452

    Google Scholar 

  • Ilg C, Oertli B (2017) Effectiveness of amphibians as biodiversity surrogates in pond conservation. Conserv Biol 31:437–445

    PubMed  Google Scholar 

  • Irwin S, Pedley SM, Coote L, Dietzsch AC, Wilson MW, Oxbrough A, Sweeney O, Moore KM, Martin R, Kelly DL, Mitchell FJ (2014) The value of plantation forests for plant, invertebrate and bird diversity and the potential for cross-taxon surrogacy. Biodivers Conserv 23:697–714

    Google Scholar 

  • Jumars PA, Dorgan KM, Lindsay SM (2015) Diet of worms emended: an update of polychaete feeding guilds. Ann Rev Mar Sci 7:497–520

    PubMed  Google Scholar 

  • Karakassis I, Machias A, Pitta P, Papadopoulou KN, Smith CJ, Apostolaki ET, Giannoulaki M, Koutsoubas D, Somarakis S (2006) Cross-community congruence of patterns in a marine ecosystem: do the parts reflect the whole? Mar Ecol Prog Ser 310:47–54

    Google Scholar 

  • Lawler JJ, White D (2008) Assessing the mechanisms behind successful surrogates for biodiversity in conservation planning. Anim Conserv 11:270–280

    Google Scholar 

  • Leroy B, Gallon R, Feunteun E, Robuchon M, Ysnel F (2017) Cross-taxon congruence in the rarity of subtidal rocky marine assemblages: no taxonomic shortcut for conservation monitoring. Ecol Indic 77:239–249

    Google Scholar 

  • Lindberg DR, Ponder WF, Haszprunar G (2004) The Mollusca: relationships and patterns from their first half-billion years. In: Cracraft J, Donoghue MJ (eds) Assembling the tree of life. Oxford University Press, New York, pp 252–278

    Google Scholar 

  • Lovell S, Hamer M, Slotow R, Herbert D (2007) Assessment of congruency across invertebrate taxa and taxonomic levels to identify potential surrogates. Biol Conserv 139:113–125

    Google Scholar 

  • MacFarlane GR, Booth DJ (2001) Estuarine macrobenthic community structure in the Hawkesbury River, Australia: relationships with sediment physicochemical and anthropogenic parameters. Environ Monit Assess 72:51–78

    CAS  PubMed  Google Scholar 

  • Magierowski RH, Johnson CR (2006) Robustness of surrogates of biodiversity in marine benthic communities. Ecol App 16:2264–2275

    Google Scholar 

  • Magurran AE (2003) Measuring biological diversity. Blackwell, Oxford

    Google Scholar 

  • Mangiafico SS (2016) Summary and analysis of extension program evaluation in R, version 1.9.0. https://www.rcompanion.org/handbook/.

  • Margules CR, Pressey RL (2000) Systematic conservation planning. Nature 405:243–253

    CAS  Google Scholar 

  • Marshall JE, Bucher DJ, Smith SD (2018) Patterns of infaunal macromollusc assemblages in a subtropical marine park: implications for management. Mar Freshwater Res 69:502–513

    Google Scholar 

  • McCune B, Mefford MJ (2018) PC-ORD. Multivariate analysis of ecological data. Version 7.08. Wild Blueberry Media, Corvallis

    Google Scholar 

  • Mellin C, Delean S, Caley J, Edgar G, Meekan M, Pitcher R, Przeslawski R, Williams A, Bradshaw C (2011) Effectiveness of biological surrogates for predicting patterns of marine biodiversity: a global meta-analysis. PLoS ONE 6:e20141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Menegotto A, Rangel TF (2018) Mapping knowledge gaps in marine diversity reveals a latitudinal gradient of missing species richness. Nat Commun 9:4713

    PubMed  PubMed Central  Google Scholar 

  • Morrisey DJ, Underwood AJ, Howitt L, Stark JS (1992) Temporal variation in soft-sediment benthos. J Exp Mar Biol Ecol 164:233–245

    Google Scholar 

  • Mueller M, Pander J, Geist J (2013) Taxonomic sufficiency in freshwater ecosystems: effects of taxonomic resolution, functional traits, and data transformation. Freshw Sci 32:762–778

    Google Scholar 

  • Neeson TM, Van Rijn I, Mandelik Y (2013) How taxonomic diversity, community structure, and sample size determine the reliability of higher taxon surrogates. Ecol App 23:1216–1225

    Google Scholar 

  • Oberprieler SK, Andersen AN, Gillespie GR, Einoder LD (2019) Vertebrates are poor umbrellas for invertebrates: cross-taxon congruence in an Australian tropical savanna. Ecosphere 10:e02755

    Google Scholar 

  • Olsgard F, Somerfield PJ (2000) Surrogates in marine benthic investigations-which taxonomic unit to target? J Aq Eco Stress Rec 7:25–42

    Google Scholar 

  • Olsgard F, Somerfield PJ, Carr MR (1997) Relationships between taxonomic resolution and data transformations in analyses of a macrobenthic community along an established pollution gradient. Mar Ecol Prog Ser 149:173–181

    Google Scholar 

  • Olsgard F, Brattegard T, Holthe T (2003) Polychaetes as surrogates for marine biodiversity: lower taxonomic resolution and indicator groups. Biodivers Conserv 12:1033–1049

    Google Scholar 

  • Padial AA, Declerck SA, De Meester LUC, Bonecker CC, Lansac-Tôha FA, Rodrigues LC, Takeda A, Train S, Velho LF, Bini LM (2012) Evidence against the use of surrogates for biomonitoring of Neotropical floodplains. Freshw Biol 57:2411–2423

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2017) nlme: linear and Nonlinear mixed effects models. https://CRAN.R-project.org/package=nlme

  • Ponder WF, Lindberg DR (eds) (2008) Phylogeny and evolution of the mollusca. University of California Press, Berkeley

    Google Scholar 

  • Przeslawski R, Radke L, Hughes M (2009) Temporal and finescale variation in the biogeochemistry of Jervis Bay. Geoscience Australia, Record 2009/12. Geoscience Australia, Canberra

  • R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Radke LC, Huang Z, Przeslawski R, Webster IT, McArthur MA, Anderson TJ, Siwabessy PJ, Brooke BP (2011) Including biogeochemical factors and a temporal component in benthic habitat maps: influences on infaunal diversity in a temperate embayment. Mar Freshwater Res 62:1432–1448

    CAS  Google Scholar 

  • Rodrigues AS, Brooks TM (2007) Shortcuts for biodiversity conservation planning: the effectiveness of surrogates. Ann Rev Ecol Evol Syst 38:713–737

    Google Scholar 

  • Rouse G, Pleijel F (2006) Reproductive biology and phylogeny of Annelida. Science Publishers, Enfield

    Google Scholar 

  • Shokri MR, Gladstone W, Kepert A (2009) Annelids, arthropods or molluscs are suitable as surrogate taxa for selecting conservation reserves in estuaries. Biodivers Conserv 18:1117–1130

    Google Scholar 

  • Smith SD (2005) Rapid assessment of invertebrate biodiversity on rocky shores: where there’s a whelk there’s a way. Biodivers Conserv 14:3565–3576

    Google Scholar 

  • Su JC, Debinski DM, Jakubauskas ME, Kindscher K (2004) Beyond species richness: community similarity as a measure of cross-taxon congruence for coarse-filter conservation. Conserv Biol 18:167–173

    Google Scholar 

  • Sutcliffe R, Pitcher CR, Caley MJ, Possingham HP (2012) Biological surrogacy in tropical seabed assemblages fails. Ecol App 22:1762–1771

    CAS  Google Scholar 

  • Sutcliffe PR, Klein CJ, Pitcher CR, Possingham HP (2015) The effectiveness of marine reserve systems constructed using different surrogates of biodiversity. Conserv Biol 29:657–667

    CAS  PubMed  Google Scholar 

  • Valesini FJ, Wildsmith MD, Tweedley JR (2018) Predicting estuarine faunal assemblages using enduring environmental surrogates, with applications in systematic conservation planning. Ocean Coast Manage 165:80–98

    Google Scholar 

  • van der Wal D, Lambert GI, Ysebaert T, Plancke YM, Herman PM (2017) Hydrodynamic conditioning of diversity and functional traits in subtidal estuarine macrozoobenthic communities. Estuar Coast Shelf Sci 197:80–92

    Google Scholar 

  • Velghe K, Gregory-Eaves I (2013) Body size is a significant predictor of congruency in species richness patterns: a meta-analysis of aquatic studies. PLoS ONE 8:e57019

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vellend M, Lilley PL, Starzomski BM (2008) Using subsets of species in biodiversity surveys. J App Ecol 45:161–169

    Google Scholar 

  • Westgate MJ, Barton PS, Lane PW, Lindenmayer DB (2014) Global meta-analysis reveals low consistency of biodiversity congruence relationships. Nat Commun 5:3899

    CAS  PubMed  Google Scholar 

  • Westgate MJ, Tulloch AI, Barton PS, Pierson JC, Lindenmayer DB (2017) Optimal taxonomic groups for biodiversity assessment: a meta-analytic approach. Ecography 40:539–548

    Google Scholar 

  • Xu G, Wang Z, Yang Z, Xu H (2015) Congruency analysis of biofilm-dwelling ciliates as a surrogate of eukaryotic microperiphyton for marine bioassessment. Mar Poll Bull 101:600–604

    CAS  Google Scholar 

  • Yong DL, Barton PS, Ikin K, Evans MJ, Crane M, Okada S, Cunningham SA, Lindenmayer DB (2018) Cross-taxonomic surrogates for biodiversity conservation in human-modified landscapes—a multi-taxa approach. Biol Conserv 224:336–346

    Google Scholar 

  • Ysebaert T, Herman PM (2002) Spatial and temporal variation in benthic macrofauna and relationships with environmental variables in an estuarine, intertidal soft-sediment environment. Mar Ecol Prog Ser 244:105–124

    Google Scholar 

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Acknowledgements

We thank the Department of Defence for funding this project through CSIRO Division of Fisheries; Libby Howitt, Angela Meza, Fiona Mackillop and Rob Patterson for assistance in the collection and sorting of samples; Ian Loch and Winston Ponder for assistance in identification of molluscs; Pauline McWilliams for assistance in identification of crustaceans and Roger Springthorpe for assistance with the decapods; Winston Ponder for assistance with the mollusc literature; and Daniel Krix for producing the map of study sites and graphs of the surrogates’ biodiversity variables. We thank the reviewers for their very helpful comments. A representative collection of the fauna is deposited in the Australian Museum.

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Authors and Affiliations

  1. Faculty of Science, University of Technology Sydney, PO Box 123, Broadway, NSW, 2007, Australia

    William Gladstone & Brad R. Murray

  2. Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW, 2010, Australia

    Pat Hutchings

  3. Department of Biological Sciences, Macquarie University, North Ryde, NSW, 2109, Australia

    Pat Hutchings

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  1. William Gladstone
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  2. Brad R. Murray
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  3. Pat Hutchings
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Correspondence to William Gladstone.

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Communicated by Angus Jackson.

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Gladstone, W., Murray, B.R. & Hutchings, P. Promising yet variable performance of cross-taxon biodiversity surrogates: a test in two marine habitats at multiple times. Biodivers Conserv 29, 3067–3089 (2020). https://doi.org/10.1007/s10531-020-02015-4

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  • DOI: https://doi.org/10.1007/s10531-020-02015-4

Keywords

  • Biodiversity assessment
  • Conservation planning
  • Ecological indicators
  • Jervis Bay
  • Posidonia
  • Species richness

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