Abstract
The effect of human activities on the suppression of biodiversity is visibly evident throughout the world. Monitoring and conservation services are usually expensive in terms of time and money, and potential savings in these areas are always welcome. The higher-taxon approach has been used as a possible alternative to overcome these impediments. However, there is little information about the effect of sample size on the effectiveness of the higher-taxon approach, mainly with empirical data. Using an extensive database, which compiles information on the distribution of ants between the years 1886 and 2020, I verified the effect of sample size on the predictive power of the higher-taxon approach in Brazil. I evaluated the effect of sample size on the predictive power of the Genus and Subfamily to represent species richness and composition at the spatial scales of State and Biomes. The associations between coarser taxonomic units and species-level are strong at both spatial scales, with metrics of richness and composition. In general, the genus has the results with the highest coefficients regardless of spatial scales. The sample size effect was sporadic and did not dramatically affect the effectiveness of the surrogates. Regardless of the possible biases that data compiled from the literature and taxonomic collections may have due to lack of standardization, coarser taxonomic units (Genus and Subfamily) were efficient predictors of species-level in Brazilian states and biomes. It reinforces the potential to save costs in monitoring and conserving ant biodiversity in a wide space-environmental gradient.
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References
Alves C, Vieira C, Almeida R, Hespanhol H (2016) Genera as surrogates of bryophyte species richness and composition. Ecol Indic 63:82–88. https://doi.org/10.1016/j.ecolind.2015.11.053
Andersen AN (1995) Measuring more of biodiversity: Genus richness as a surrogate for species in Australian ant faunas. Biol Conserv 73:39–43. https://doi.org/10.1016/0006-3207(95)90059-4
Andersen AN, Hoffmann BD, Müller WJ, Griffiths AD (2002) Using ants as bioindicators in land management: simplifying assessment of ant community responses. J Appl Ecol 39:8–17. https://doi.org/10.1046/j.1365-2664.2002.00704.x
Andrade-Silva J, Baccaro FB, Prado LP et al (2022) A large-scale assessment of ant diversity across the Brazilian Amazon Basin: integrating geographic, ecological and morphological drivers of sampling bias. Ecography (cop). https://doi.org/10.1111/ecog.06295
Auguie B (2017) gridExtra: Miscellaneous Functions for "Grid" Graphics. R package version 2.3, Available at: https://CRAN.R-project.org/package=gridExtra. Accessed 23 Aug 2022
Balian EV, Drius L, Eggermont H et al (2016) Supporting evidence-based policy on biodiversity and ecosystem services: Recommendations for effective policy briefs. Evid Policy 12:431–451. https://doi.org/10.1332/174426416X14700777371551
Barlow J, Lennox GD, Ferreira J et al (2016) Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation. Nature 535:144–147. https://doi.org/10.1038/nature18326
Bevilacqua S, Terlizzi A, Claudet J et al (2012) Taxonomic relatedness does not matter for species surrogacy in the assessment of community responses to environmental drivers. J Appl Ecol 49:357–366. https://doi.org/10.1111/j.1365-2664.2011.02096.x
Bhusal DR, Kallimanis AS, Tsiafouli MA, Sgardelis SP (2014) Higher taxa vs. functional guilds vs. trophic groups as indicators of soil nematode diversity and community structure. Ecol Indic 41:25–29. https://doi.org/10.1016/j.ecolind.2014.01.019
Bilton DT, Mcabendroth L, Bedford A, Ramsay PM (2006) How wide to cast the net? Cross-taxon congruence of species richness, community similarity and indicator taxa in ponds. Freshw Biol 51:578–590. https://doi.org/10.1111/j.1365-2427.2006.01505.x
Bissonette JA (1999) Small sample size problems in wildlife ecology: A contingent analytical approach. Wildlife Biol 5:65–71. https://doi.org/10.2981/wlb.1999.010
Bivand R, Keitt T, Rowlingson B (2022) rgdal: Bindings for the 'Geospatial' Data Abstraction Library. R package version 1.6-2, Available at: https://CRAN.R-project.org/package=rgdal. Accessed 23 Aug 2022
Bockmann FA, Rodrigues MT, Kohsldorf T et al (2018) Brazil’s government attacks biodiversity. Science 360:865. https://doi.org/10.1126/science.aat7540
Butchart SHM, Walpole M, Collen B et al (2010) Global biodiversity: indicators of recent declines. Science 80(328):1164–1168. https://doi.org/10.1126/science.1187512
Cardoso P, Silva I, de Oliveira NG, Serrano ARM (2004a) Indicator taxa of spider (Araneae) diversity and their efficiency in conservation. Biol Conserv 120:517–524. https://doi.org/10.1016/j.biocon.2004.03.024
Cardoso P, Silva I, Oliveira NG, Serrano ARM (2004b) Higher taxa surrogates of spider (Araneae) diversity and their efficiency in conservation. Biol Conserv 117:453–459. https://doi.org/10.1016/j.biocon.2003.08.013
Carneiro FM, Bini LM, Rodrigues LC (2010) Influence of taxonomic and numerical resolution on the analysis of temporal changes in phytoplankton communities. Ecol Indic 10:249–255. https://doi.org/10.1016/j.ecolind.2009.05.004
Caro TM (2010) Conservation by Proxy: Indicator, umbrella, keystone, flagship, and other surrogate species. Island Press, Washington
Caro T, Rowe Z, Berger J et al (2022) An inconvenient misconception: Climate change is not the principal driver of biodiversity loss. Conserv Lett. https://doi.org/10.1111/conl.12868
Caruso T, Migliorini M (2006) Micro-arthropod communities under human disturbance: is taxonomic aggregation a valuable tool for detecting multivariate change? Evidence from Mediterranean soil oribatid coenoses. Acta Oecologica 30:46–53. https://doi.org/10.1016/j.actao.2006.01.003
Ceballos G, Ehrlich PR, Dirzo R (2017) Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc Natl Acad Sci USA 114:E6089–E6096. https://doi.org/10.1073/pnas.1704949114
Costa FRC, Magnusson WE (2010) The need for large-scale, integrated studies of biodiversity—the experience of the program for biodiversity research in Brazilian Amazonia. Nat Conserv 08:3–12. https://doi.org/10.4322/natcon.00801001
Dale MB, Clifford HT (1976) On the effectiveness of higher taxonomic ranks for vegetation analysis. Aust J Ecol 1:37–62. https://doi.org/10.1111/j.1442-9993.1976.tb01091.x
de Oliveira Andrade R (2019) Brazil budget cuts threaten 80,000 science scholarships. Nature 572:575–576. https://doi.org/10.7748/eldc.7.5.9.s8
Solar RRC, Barlow J, Andersen AN et al (2016) Biodiversity consequences of land-use change and forest disturbance in the Amazon: A multi-scale assessment using ant communities. Biol Conserv 197:98–107. https://doi.org/10.1016/j.biocon.2016.03.005
Dixon PM, Garrett KA (1993) Sampling ecological information: choice of sample size, reconsidered. Ecol Modell 68:67–73. https://doi.org/10.1016/0304-3800(93)90108-5
dos Santos Ribas LG, Padial AA (2015) The use of coarser data is an effective strategy for biological assessments. Hydrobiologia 747:83–95. https://doi.org/10.1007/s10750-014-2128-6
Driessen MM, Kirkpatrick JB (2019) Higher taxa can be effective surrogates for species-level data in detecting changes in invertebrate assemblage structure due to disturbance: a case study using a broad range of orders. Austral Entomol 58:361–369. https://doi.org/10.1111/aen.12315
Durant SM, Groom R, Kuloba B et al (2019) Bridging the divide between scientists and decision-makers: How behavioural ecologists can increase the conservation impact of their research? Philos Trans R Soc B. https://doi.org/10.1098/rstb.2019.0011
Dytham C (2011) Choosing and using statistics : a biologist’s guide, 3rd edn. Wiley-Blackwell, Chichester
Ellis D (1985) Taxonomic sufficiency in pollution assessment. Mar Pollut Bull 16:459. https://doi.org/10.1016/0025-326X(85)90362-5
Escobar H (2019) Brazilian scientists lament ‘freeze’ on research budget. Science 364:111. https://doi.org/10.1126/science.364.6436.111
Feitosa RM, Camacho GP, Silva TSR et al (2022) Ants of Brazil: an overview based on 50 years of diversity studies. Syst Biodivers 20:2089268. https://doi.org/10.1080/14772000.2022.2089268
Fernandes GW, Vale MM, Overbeck GE et al (2017) Dismantling Brazil’s science threatens global biodiversity heritage. Perspect Ecol Conserv 15:239–243. https://doi.org/10.1016/j.pecon.2017.07.004
Gallego I, Davidson T, a., Jeppesen E, et al (2012) Taxonomic or ecological approaches? Searching for phytoplankton surrogates in the determination of richness and assemblage composition in ponds. Ecol Indic 18:575–585. https://doi.org/10.1016/j.ecolind.2012.01.002
Gardner TA, Barlow J, Araujo IS et al (2008) The cost-effectiveness of biodiversity surveys in tropical forests. Ecol Lett 11:139–150. https://doi.org/10.1111/j.1461-0248.2007.01133.x
Gaspar C, Gaston KJ, Borges PAV (2010) Arthropods as surrogates of diversity at different spatial scales. Biol Conserv 143:1287–1294. https://doi.org/10.1016/j.biocon.2010.03.007
Gaston KJ (2000) Biodiversity: higher taxon richness. Prog Phys Geogr 24:117–127. https://doi.org/10.1177/030913330002400108
Gaston KJ, Williams PH (1993) Mapping the world’s species-The higher taxon approach. Biodivers Lett 1:2–8. https://doi.org/10.2307/2999642
Gonçalves-Souza D, Vilela B, Phalan B, Dobrovolski R (2021) The role of protected areas in maintaining natural vegetation in Brazil. Sci Adv. https://doi.org/10.1126/sciadv.abh2932
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391. https://doi.org/10.1046/j.1461-0248.2001.00230.x
Gotelli NJ, Ellison AM (2013) A Primer of Ecological Statistics, 2nd edn. Sinauer Associates, Sunderland
Groc S, Delabie JHC, Longino JT et al (2010) A new method based on taxonomic sufficiency to simplify studies on Neotropical ant assemblages. Biol Conserv 143:2832–2839. https://doi.org/10.1016/j.biocon.2010.07.034
Habel JC, Rasche L, Schneider UA et al (2019) Final countdown for biodiversity hotspots. Conserv Lett. https://doi.org/10.1111/conl.12668
Hawkins BA, Field R, Cornell HV et al (2003) Energy, water, and broad-scale geographic patterns of species richness. Ecology 84:3105–3117. https://doi.org/10.1890/03-8006
Heino J, Soininen J (2007) Are higher taxa adequate surrogates for species-level assemblage patterns and species richness in stream organisms? Biol Conserv 137:78–89. https://doi.org/10.1016/j.biocon.2007.01.017
Hijmans R (2022) raster: Geographic Data Analysis and Modeling. R package version 3.6-3, Available at: https://CRAN.R-project.org/package=raster. Accessed 23 Aug 2022
Hipólito J, Shirai LT, Diele-Viegas LM et al (2021) Brazilian budget cuts further threaten gender equality in research. Nat Ecol Evol 26947:20201292. https://doi.org/10.1038/s41559-021-01640-8
IBGE (2016) Mapa de Biomas e de Vegetação. Ministério do Planejamento, Orçamento e Gestão. Available at: http://mapas.ibge.gov.br/. Accessed 28 Oct 2020
Jones FC (2008) Taxonomic sufficiency: The influence of taxonomic resolution on freshwater bioassessments using benthic macroinvertebrates. Environ Rev 16:45–69. https://doi.org/10.1139/A07-010
Koch EBA, Nascimento IC, Majer JD, Delabie JHC (2021) Seeking surrogates for taxonomic and functional evaluations of leaf-litter ant faunas. Ecol Indic 122:107305. https://doi.org/10.1016/j.ecolind.2020.107305
Kowaltowski AJ (2021) Brazil’s scientists face 90% budget cut. Nature 598:566. https://doi.org/10.1038/d41586-021-02882-z
Krzywinski M, Altman N (2013) Points of significance: power and sample size. Nat Methods 10:1139–1140. https://doi.org/10.1038/nmeth.2738
Lawler JJ, White D (2008) Assessing the mechanisms behind successful surrogates for biodiversity in conservation planning. Anim Conserv 11:270–280. https://doi.org/10.1111/j.1469-1795.2008.00176.x
Lawton JH, Bignell DE, Bolton B et al (1998) Biodiversity inventories, indicator taxa and effects of habitat modification in tropical forest. Nature 391:72–75. https://doi.org/10.1038/34166
Lewinsohn TM, Agostini K, LucciFreitas AV, Melo AS (2022) Insect decline in Brazil: an appraisal of current evidence. Biol Lett. https://doi.org/10.1098/rsbl.2022.0219
Loecher M, Ropkins K (2015) RgoogleMaps and loa: Unleashing R Graphics Power on Map Tiles. J Stat Soft 63(4):1–18. https://doi.org/10.18637/jss.v063.i04
Longino JT, Colwell RK (1997) Biodiversity assessment using structured inventory: capturing the ant fauna of a tropical rain forest. Ecol Appl 7:1263–1277. https://doi.org/10.2307/2641213
Magurran AE, Baillie SR, Buckland ST et al (2010) Long-term datasets in biodiversity research and monitoring: Assessing change in ecological communities through time. Trends Ecol Evol 25:574–582. https://doi.org/10.1016/j.tree.2010.06.016
Margules CR, Pressey RL (2000) Systematic conservation planning. Nature 405:243–253. https://doi.org/10.1038/35012251
McDonald JH (2014) Handbook of Biological Statistics, 3rd edn. Sparky House Publishing, Baltimore
Murphy KR, Myors B (2004) Statistical Power Analysis, 2nd edn. Lawrence Erlbaum Associates, Mahwah
Nakamura A, Catterall CP, House APN et al (2007) The use of ants and other soil and litter arthropods as bio-indicators of the impacts of rainforest clearing and subsequent land use. J Insect Conserv 11:177–186. https://doi.org/10.1007/s10841-006-9034-9
Neeson TM, Van Rijn I, Mandelik Y (2013) How taxonomic diversity, community structure, and sample size determine the reliability of higher taxon surrogates. Ecol Appl 23:1216–1225. https://doi.org/10.1890/12-1167.1
Oksanen J, Simpson G, Blanchet F, et al (2022) vegan: Community Ecology Package (R package version 2.6-2). Available at: https://cran.r-project.org/package=vegan. Accessed 23 Aug 2022
Oliver I, Beattie AJ (1993) A possible method for the rapid assessment of biodiversity. Conserv Biol 7:562–568. https://doi.org/10.1046/j.1523-1739.1993.07030562.x
Oliver I, Beattie AJ (1996) Designing a cost-effective invertebrate survey: a test of methods for rapid assessment of biodiversity. Ecol Appl 6:594–607. https://doi.org/10.2307/2269394
Peres-Neto P, Jackson D (2001) How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia 129:169–178. https://doi.org/10.1007/s004420100720
Pik AJ, Oliver I, Beattie AJ (1999) Taxonomic sufficiency in ecological studies of terrestrial invertebrates. Aust J Ecol 24:555–562. https://doi.org/10.1046/j.1442-9993.1999.01003.x
Prance GT (1994) A Comparison of the efficacy of higher taxa and species numbers in the assessment of biodiversity in the neotropics. Philos Trans R Soc Lond B 345:89–99. https://doi.org/10.1098/rstb.1994.0090
Pullin AS, Knight TM (2003) Support for decision making in conservation practice: An evidence-based approach. J Nat Conserv 11:83–90. https://doi.org/10.1078/1617-1381-00040
Queiroz ACM, Marques TG, Ribas CR et al (2022) Ant diversity decreases during the dry season: A meta-analysis of the effects of seasonality on ant richness and abundance. Biotropica. https://doi.org/10.1111/btp.13158
R Core Team (2022) A language and environment for statistical computing.Vienna, Austria. Available at: R Foundation for Statistical Computing.https://www.r-project.org/. Accessed 23 Aug 2022
Rahbek C (2005) The role of spatial scale and the perception of large-scale species-richness patterns. Ecol Lett 8:224–239. https://doi.org/10.1111/j.1461-0248.2004.00701.x
Ricketts TH, Daily GC, Ehrlich PR (2002) Does butterfly diversity predict moth diversity? Testing a popular indicator taxon at local scales. Biol Conserv 103:361–370. https://doi.org/10.1016/S0006-3207(01)00147-1
Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 80(235):167–171. https://doi.org/10.1126/science.235.4785.167
Ripple WJ, Wolf C, Newsome TM et al (2021) World scientists’ warning of a climate emergency 2021. Bioscience 71:894–898. https://doi.org/10.1093/biosci/biab079
Rosser N (2017) Shortcuts in biodiversity research: What determines the performance of higher taxa as surrogates for species? Ecol Evol 7:2595–2603. https://doi.org/10.1002/ece3.2736
Rosser N, Eggleton P (2012) Can higher taxa be used as a surrogate for species-level data in biodiversity surveys of litter/soil insects? J Insect Conserv 16:87–92. https://doi.org/10.1007/s10841-011-9395-6
Sætersdal M, Gjerde I, Blom HH (2005) Indicator species and the problem of spatial inconsistency in nestedness patterns. Biol Conserv 122:305–316. https://doi.org/10.1016/j.biocon.2004.07.020
Schmidt FA, Ribas CR, Feitosa RM et al (2022) Ant diversity studies in Brazil: an overview of the myrmecological research in a megadiverse country. Insectes Soc 69:105–121. https://doi.org/10.1007/s00040-022-00848-
Silva RR, Martello F, Feitosa RM et al (2022) ATLANTIC ANTS: a data set of ants in Atlantic Forests of South America. Ecology 103:1–5. https://doi.org/10.1002/ecy.3580
Singh AS, Masuku MB (2014) Sampling techniques and determination of sample size in applied statistics research: An overview. Int J Econ Commer Manag II:1–22
Souza JLP, Fernandes IO (2021) Do spatial and temporal scales affect the efficiency of surrogates in ant monitoring on the hydroelectric power-plant area in Brazilian Amazon? Ecol Indic 121:107158. https://doi.org/10.1016/j.ecolind.2020.107158
Souza JLP, Baccaro FB, Landeiro VL et al (2016) Taxonomic sufficiency and indicator taxa reduce sampling costs and increase monitoring effectiveness for ants. Divers Distrib 22:111–122. https://doi.org/10.1111/ddi.12371
Souza JLP, Baccaro FB, Pequeno PACL et al (2018) Effectiveness of genera as a higher-taxon substitute for species in ant biodiversity analyses is not affected by sampling technique. Biodivers Conserv 27:3425–3445. https://doi.org/10.1007/s10531-018-1607-x
Souza JLP, Fernandes IO, Agosti D et al (2022) Assessing the efficacy of higher-taxon approach for ant species surveys to improve biodiversity inventories. Anim Conserv 25:370–381. https://doi.org/10.1111/acv.12758
Spiesman BJ, Cumming GS (2008) Communities in context: The influences of multiscale environmental variation on local ant community structure. Landsc Ecol 23:313–325. https://doi.org/10.1007/s10980-007-9186-3
Strand M, Panova M (2015) Size of genera—biology or taxonomy? Zool Scr 44:106–116. https://doi.org/10.1111/zsc.12087
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. https://doi.org/10.1111/j.1523-1739.2004.00337.x
Van Rijn I, Neeson TM, Mandelik Y (2015) Reliability and refinement of the higher taxa approach for bee richness and composition assessments. Ecol Appl 25:88–98. https://doi.org/10.1890/13-2380.1
Whittaker RJ, Araújo MB, Jepson P et al (2005) Conservation biogeography: assessment and prospect. Divers Distrib 11:3–23. https://doi.org/10.1111/j.1366-9516.2005.00143.x
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, Cham
Williams PH, Gaston KHJ (1994) Measuring more of diversity: Can higher-taxon richness predict wholesale species richness? Biol Conserv 67:211–217. https://doi.org/10.1016/0006-3207(94)90612-2
Wisz MS, Hijmans RJ, Li J et al (2008) Effects of sample size on the performance of species distribution models. Divers Distrib 14:763–773. https://doi.org/10.1111/j.1472-4642.2008.00482.x
Acknowledgements
This study was supported by the National Council for Scientific and Technological Development (CNPq, Programa de Capacitação Institucional—PCI/INMA) of the Brazilian Ministry of Science, Technology and Innovation (MCTI). I thank the coordination and the members of the sub-project Conservation of Biodiversity in the Central Atlantic Forest (PCI-1) for their unconditional support in the elaboration of this manuscript. Thanks also to Ana C. Loss for her help in extracting geographic data from the rasters using R. I was supported by a CNPq PCI/INMA (300886/2022-5) post-doctoral scholarship.
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The funding was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq PCI/INMA (Grant No. 302065/2021-0).
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JLPS defined the conception and design of the study. JLPS prepared the material and analyzed the data. JLPS wrote the first version of the manuscript and prepared the figures and tables present in the current version of this manuscript.
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10531_2022_2516_MOESM2_ESM.xlsx
Supplementary file2 (XLSX 12 KB)—Online Resource 2. Values of Species (added to the morphospecies), Genus and Subfamily richness; regression coefficients of richness and composition and the species:higher-taxon ratio for the states and biomes spatial scales tested in Brazil.
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Supplementary file3 (PDF 19 KB)—Online Resource 3. Regression between the sample size and numbers of Species, Genera and Subfamilies of ants for States and Biomes grains of the spatial scale in the Brazil. The regressions were significant at P < 0.01.
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Souza, J.L.P. Effectiveness of higher-taxon approach on ants and sample size effect: an assessment in Brazilian biomes and states. Biodivers Conserv 32, 635–652 (2023). https://doi.org/10.1007/s10531-022-02516-4
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DOI: https://doi.org/10.1007/s10531-022-02516-4