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Research Article

Never underestimate biodiversity: how undersampling affects Bray–Curtis similarity estimates and a possible countermeasure

ORCID Icon & ORCID Icon
Pages 660-672 | Received 18 Jan 2023, Accepted 08 Aug 2023, Published online: 14 Sep 2023

References

  • Anderson MJ. 2017. Permutational multivariate analysis of variance (PERMANOVA). In: Balakrishnan N, Colton T, Everitt B, et al., editors. Wiley StatsRef: Statistics reference online. Chichester, UK: John Wiley & Sons, Ltd. pp. 1–15.
  • Anderson MJ, Crist TO, Chase JM, Vellend M, Inouye BD, Freestone AL, Sanders NJ, Cornell HV, Comita LS, Davies KF, Harrison SP, Kraft NJB, Stegen JC, Swenson NG. 2011. Navigating the multiple meanings of β diversity: A roadmap for the practicing ecologist. Ecology Letters 14:19–28. DOI: 10.1111/j.1461-0248.2010.01552.x.
  • Andresen E. 2003. Effect of forest fragmentation on dung beetle communities and functional consequences for plant regeneration. Ecography 26:87–97. DOI: 10.1034/j.1600-0587.2003.03362.x.
  • Bacaro G, Gioria M, Ricotta C. 2012. Testing for differences in beta diversity from plot-to-plot dissimilarities. Ecological Research 27:285–292. DOI: 10.1007/s11284-011-0899-z.
  • Barwell LJ, Isaac NJB, Kunin WE. 2015. Measuring β diversity with species abundance data. The Journal of Animal Ecology 84:1112–1122. DOI: 10.1111/1365-2656.12362.
  • Battaglia M, Hose GC, Turak E, Warden B. 2005. Depauperate macroinvertebrates in a mine affected stream: Clean water may be the key to recovery. Environmental Pollution 138:132–141. DOI: 10.1016/j.envpol.2005.02.022.
  • Beck J, Holloway JD, Schwanghart W. 2013. Undersampling and the measurement of beta diversity. Methods in Ecology and Evolution / British Ecological Society 4:370–382. DOI: 10.1111/2041-210x.12023.
  • Beck J, Schwanghart W. 2010. Comparing measures of species diversity from incomplete inventories: An update. Methods in Ecology and Evolution 1:38–44. DOI: 10.1111/j.2041-210X.2009.00003.x.
  • Bittinger K. 2020. abdiv: Alpha and beta diversity measures. R package version 0.2.0. Available: https://CRAN.R-project.org/package=abdiv.
  • Bloom S. 1981. Similarity indices in community studies: Potential pitfalls. Marine Ecology Progress Series 5:125–128. DOI: 10.3354/meps005125.
  • Bonham KJ, Mesibov R, Bashford R. 2002. Diversity and abundance of some ground-dwelling invertebrates in plantation vs. native forests in Tasmania, Australia. Forest Ecology and Management 158:237–247. DOI: 10.1016/S0378-1127(00)00717-9.
  • Borcard D, Gillet F, Legendre P. 2011. Numerical ecology with R. New York, NY: Springer Verlag. pp. 306.
  • Boulton AM, Davies KF, Ward PS. 2005. Species richness, abundance, and composition of ground-dwelling ants in Northern California grasslands: Role of plants, soil, and grazing. Environmental Entomology 34:96–104. DOI: 10.1603/0046-225X-34.1.96.
  • Bray JR, Curtis JT. 1957. An ordination of the upland forest communities of Southern Wisconsin. Ecological Monographs 27:325–349. DOI: 10.2307/1942268.
  • Cao Y, Larsen DP, Hughes RM. 2001. Evaluating sampling sufficiency in fish assemblage surveys: A similarity-based approach. Canadian Journal of Fisheries and Aquatic Sciences 58:1782–1793. DOI: 10.1139/f01-120.
  • Cardoso P, Borges PAV, Veech JA. 2009. Testing the performance of beta diversity measures based on incidence data: The robustness to undersampling. Diversity & Distributions 15:1081–1090. DOI: 10.1111/j.1472-4642.2009.00607.x.
  • Chao A, Chazdon RL, Colwell RK, Shen TJ. 2005. A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecology Letters 8:148–159. DOI: 10.1111/j.1461-0248.2004.00707.x.
  • Chao A, Chazdon RL, Colwell RK, Shen TJ. 2006. Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62:361–371. DOI: 10.1111/j.1541-0420.2005.00489.x.
  • Chao A, Hsieh TC, Chazdon RL, Colwell RK, Gotelli NJ. 2015. Unveiling the species-rank abundance distribution by generalizing the Good-Turing sample coverage theory. Ecology 96:1189–1201. DOI: 10.1890/14-0550.1.
  • Chapman MG. 2002. Patterns of spatial and temporal variation of macrofauna under boulders in a sheltered Boulder field. Austral Ecology 27:211–228. DOI: 10.1046/j.1442-9993.2002.01172.x.
  • Chumak V, Obrist MK, Moretti M, Duelli P. 2015. Arthropod diversity in pristine vs. managed beech forests in Transcarpathia (Western Ukraine). Global Ecology and Conservation 3:72–82. DOI: 10.1016/j.gecco.2014.11.001.
  • Clarke KR, Somerfield PJ, Chapman MG. 2006. On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. Journal of Experimental Marine Biology and Ecology 330:55–80. DOI: 10.1016/j.jembe.2005.12.017.
  • Clarke KR, Warwick RM. 2001. Change in marine communities: An approach to statistical analysis and interpretation. 2nd ed. Plymouth: PRIMER-E.
  • Collier KJ, Smith BJ, Baillie BR. 1997. Summer light‐trap catches of adult Trichoptera in hill‐country catchments of contrasting land use, Waikato, New Zealand. New Zealand Journal of Marine and Freshwater Research 31:623–634. DOI: 10.1080/00288330.1997.9516794.
  • Colwell RK, Coddington JA. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society B 311:118–345.
  • Filloy J, Grosso S, Bellocq MI. 2015. Urbanization altered latitudinal patterns of bird diversity-environment relationships in the southern Neotropics. Urban Ecosyst 18:777–791. DOI: 10.1007/s11252-014-0429-1.
  • Gaston KJ, Spicer JI. 2004. Biodiversity: An introduction. 2nd ed. Malden, USA: Blackwell Publishing. pp. 191.
  • Goslee SC, Urban DL. 2007. The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22(7):1–19. DOI: 10.18637/jss.v022.i07.
  • Gower JC, Legendre P. 1986. Metric and Euclidean properties of dissimilarity coefficients. Journal of Classification 3:5–48. DOI: 10.1007/BF01896809.
  • Gristina M, Bahri T, Fiorentino F, Garofalo G. 2006. Comparison of demersal fish assemblages in three areas of the Strait of Sicily under different trawling pressure. Fisheries Research 81:60–71. DOI: 10.1016/j.fishres.2006.05.010.
  • Hardersen S, Corezzola S, Gheza G, Dell’Otto A, La Porta G. 2017. Sampling and comparing odonate assemblages by means of exuviae: Statistical and methodological aspects. Journal of Insect Conservation 21:207–218. DOI: 10.1007/s10841-017-9969-z.
  • Hardersen S, Curletti G, Leseigneur L, Platia G, Liberti G, Leo P, Cornacchia P, Gatti E. 2014. Spatio-temporal analysis of beetles from the canopy and ground layer in an Italian lowland forest. Bulletin of Insectology 67:87–97.
  • Heck KL, Able KW, Roman CT, Fahay MP. 1995. Composition, abundance, biomass, and production of macrofauna in a New England estuary: Comparisons among eelgrass meadows and other nursery habitats. Estuaries 18:379. DOI: 10.2307/1352320.
  • Horváth B, Tóth V, Kovács G. 2013. The effect of herb layer on nocturnal Macrolepidoptera (Lepidoptera: Macroheterocera) communities. Acta Silvatica et Lignaria Hungarica 9:43–56. DOI: 10.2478/aslh-2013-0004.
  • Jokimäki J, Kaisanlahti-Jokimäki ML. 2003. Spatial similarity of urban bird communities: A multiscale approach. Journal of Biogeography 30:1183–1193. DOI: 10.1046/j.1365-2699.2003.00896.x.
  • Jost L, Chao A, Chazdon RL. 2011. Compositional similarity and β (beta) diversity. In: Magurran AE, McGill BJ, editors. Biological diversity – Frontiers in measurement and assessment. Oxford: Oxfard University Press. pp. 66–84.
  • Jurasinski G, Retzer V, Beierkuhnlein C. 2009. Inventory, differentiation, and proportional diversity: A consistent terminology for quantifying species diversity. Oecologia 159:15–26. DOI: 10.1007/s00442-008-1190-z.
  • Kindt R, Coe R. 2005. Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. Nairobi: World Agroforestry Centre (ICRAF). pp. 196.
  • Legendre P, De Cáceres M. 2013. Beta diversity as the variance of community data: Dissimilarity coefficients and partitioning. Ecology Letters 16:951–963. DOI: 10.1111/ele.12141.
  • Legendre P, Gallagher ED. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280. DOI: 10.1007/s004420100716.
  • Logan M. 2010. Biostatistical design and analysis using R: A practical guide. Chichester, West Sussex: Wiley-Blackwell. pp. 546.
  • Luja VH, Herrando-Pérez S, González-Solís D, Luiselli L. 2008. Secondary rain forests are not havens for reptile species in tropical Mexico. Biotropica 40:747–757. DOI: 10.1111/j.1744-7429.2008.00439.x.
  • Maes D, Vanreusel W, Herremans M, Vantieghem P, Brosens D, Gielen K, Beck O, Van Dyck H, Desmet P, Natuurpunt V. 2016. A database on the distribution of butterflies (Lepidoptera) in northern Belgium (Flanders and the Brussels Capital Region). ZooKeys 585:143–156. DOI: 10.3897/zookeys.585.8019.
  • Magurran AE. 2004. Measuring biological diversity. Malden, USA: Blackwell Publishing. pp. 256.
  • Marriott FHC. 1990. A dictionary of statistical terms. 5th ed. Harlow, Essex: Longman Publishing Group. pp. 223.
  • Melo AS. 2021. Heavy-weighting rare species in dissimilarity indices improve recovery of multivariate groups. Ecological Complexity 46:100925. DOI: 10.1016/j.ecocom.2021.100925.
  • Meredith M. 2020. wiqid: Quick and dirty estimates for wildlife populations. R package version 0.2.3. Available: https://CRAN.R-project.org/package=wiqid.
  • Minchin PR. 1987. An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69:89–107. DOI: 10.1007/BF00038690.
  • Mueter FJ, Norcross BL. 2000. Species composition and abundance of juvenile groundfishes around Steller Sea Lion Eumetopias jubatus rookeries in the Gulf of Alaska. Alaska Fishery Research Bulletin 7:33–43.
  • Muturi EJ, Shililu J, Jacob B, Gu W, Githure J, Novak R. 2006. Mosquito species diversity and abundance in relation to land use in a riceland agroecosystem in Mwea, Kenya. Journal of Vector Ecology 31:129–137. DOI: 10.3376/1081-1710(2006)31[129:MSDAAI]2.0.CO;2.
  • Niemelä J, Kotze DJ, Venn S, Penev L, Stoyanov I, Spence J, Hartley D, De Oca EM. 2002. Carabid beetle assemblages (Coleoptera, Carabidae) across urban-rural gradients: An international comparison. Landscape Ecology 17:387–401. DOI: 10.1023/A:1021270121630.
  • Oksanen J. 2016. Multivariate analysis of ecological communities in R: Vegan tutorial. Available: http://cc.oulu.fi/~jarioksa/opetus/metodi/vegantutor.pdf.
  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H. 2019. Package vegan: Community ecology package. Version 2(5–6):296.
  • Pruim RD, Kaplan T, J Horton NJ. 2017. The mosaic package: Helping students to ‘Think with data’ using R. The R Journal 9(1):77–102. DOI: 10.32614/RJ-2017-024.
  • R Core Team. 2022. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available: https://www.R-project.org/.
  • Ricotta C, Podani J. 2017. On some properties of the Bray-Curtis dissimilarity and their ecological meaning. Ecological Complexity 31:201–205. DOI: 10.1016/j.ecocom.2017.07.003.
  • Schmera D, Eros T. 2006. Estimating sample representativeness in a survey of stream caddisfly fauna. Annales de Limnologie-International Journal of Limnology 42(3):181–187. DOI: 10.1051/limn/2006019.
  • Schneck F, Melo AS. 2010. Reliable sample sizes for estimating similarity among macroinvertebrate assemblages in tropical streams. Annales de Limnologie-International Journal of Limnology 46(2):93–100. DOI: 10.1051/limn/2010013.
  • Schroeder PJ, Jenkins DG. 2018. How robust are popular beta diversity indices to sampling error. Ecosphere 9:1–14. DOI: 10.1002/ecs2.2100.
  • Shah PA, Brooks DR, Ashby JE, Perry JN, Woiwod IP. 2003. Diversity and abundance of the coleopteran fauna from organic and conventional management systems in southern England. Forest Agriculture Enterprises 5:51–60. DOI: 10.1046/j.1461-9563.2003.00162.x.
  • Stark JS, Riddle MJ, Simpson RD. 2003. Human impacts in soft-sediment assemblages at Casey Station, East Antarctica: Spatial variation, taxonomic resolution and data transformation. Austral Ecology 28:287–304. DOI: 10.1046/j.1442-9993.2003.01289.x.
  • Stevens T, Connolly RM. 2005. Local-scale mapping of benthic habitats to assess representation in a marine protected area. Marine and Freshwater Research 56:111. DOI: 10.1071/MF04233.
  • Thorn S, Bässler C, Gottschalk T, Hothorn T, Bussler H, Raffa K, Müller J. 2014. New insights into the consequences of post-windthrow salvage logging revealed by functional structure of saproxylic beetles assemblages. PLoS ONE 9:7. DOI: 10.1371/journal.pone.0101757.
  • Walther BA, Moore JL. 2005. The concepts of bias, precision and accuracy, and their use in testing the performance of species richness estimators, with a literature review of estimator performance. Ecography 28:815–829. DOI: 10.1111/j.2005.0906-7590.04112.x.
  • Wetzel CE, Bicudo DDC, Ector L, Lobo EA, Soininen J, Landeiro VL, Bini LM. 2012. Distance decay of similarity in neotropical diatom communities. PLoS ONE 7:e45071. DOI: 10.1371/journal.pone.0045071.
  • Wickham H. 2016. ggplot2: Elegant graphics for data analysis. New York: Springer-Verlag.
  • Zou Y, Axmacher JC. 2019. The Chord-Normalized Expected Species Shared (CNESS)-Distance represents a superior measure of species turnover patterns. Methods in Ecology and Evolution / British Ecological Society 11:273–280. DOI: 10.1111/2041-210X.13333.