Abstract
Rarity is an important aspect of biodiversity often neglected in ecological studies. Species abundance distributions (SADs) are useful tools to describe patterns of commonness–rarity in ecological communities. Most studies assume field observations of species relative abundances are approximately equal to their true relative abundances, thus dismissing the potential for, and importance of unseen rare species. Here, we adopted the approach proposed by Chao et al. (Ecol, 96:1189–1201, 2015) to estimate the number and abundance of unseen species, and thus the true SADs, for tree species in 48 forest sites in Minas Gerais state, Brazil (4 rainforests, 35 semideciduous forests, and 9 deciduous forests). Also, we assessed the correlations between both unseen and rare species and sampling protocol and environment characteristics (climate, terrain, terrain heterogeneity). We found estimated true SADs invariably had higher species richness values than observed in the surveys, due to the increase in rare species. We estimate that up to 55.6% of tree species per site were unseen (8.5–55.6%), with an average of 26.6%. The estimated percentage of rare species per site was between 31.9% and 72.8%, with an average of 57.78%. We found rarity to be most strongly correlated with the percentage of unidentified trees, local terrain conditions and heterogeneity at site-level. Semideciduous forest and rainforest had similar higher percentages of unseen species (c. 27.2%) when compared to deciduous forests, probably due to the relatively higher local heterogeneity of these forests, which may provide more niches for rare species. Future studies should consider estimating true species abundances to better assess biodiversity.
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Albuquerque, U. P., Araújo, E. L., El-Deir, A. C. A. L., Souto, A., Bezerra, B. M., Ferraz, E. M. N., et al. (2012). Caatinga revisited: Ecology and conservation of an important seasonal dry forest. The Scientific World Journal, 2012, 1–18. https://doi.org/10.1100/2012/205182.
Archaux, F., Camaret, S., Dupouey, J.-L., Ulrich, E., Corcket, E., Bourjot, L., et al. (2009). Can we reliably estimate species richness with large plots? an assessment through calibration training. Plant Ecology, 203, 303–315. https://doi.org/10.1007/s11258-008-9551-6.
Arellano, G., Umaña, M. N., Macía, M. J., Loza, M. I., Fuentes, A., Cala, V., et al. (2017). The role of niche overlap, environmental heterogeneity, landscape roughness and productivity in shaping species abundance distributions along the Amazon-Andes gradient. Global Ecology Biogeography, 26, 191–202. https://doi.org/10.1111/geb.12531.
Béguinot, J. (2018). Numerical extrapolation of the species abundance distribution unveils the true species richness and the hierarchical structuring of a partially sampled marine gastropod community in the Andaman Islands (India). Asian Journal of Environment and Ecology, 6, 1–23. https://doi.org/10.9734/ajee/2018/41293.
Berdugo, M., Maestre, F. T., Kéfi, S., Gross, N., Le Bagousse-Pinguet, Y., & Soliveres, S. (2019). Aridity preferences alter the relative importance of abiotic and biotic drivers on plant species abundance in global drylands. Journal of Ecology, 107, 190–202. https://doi.org/10.1111/1365-2745.13006.
Boyle, B., Hopkins, N., Lu, Z., Raygoza Garay, J. A., Mozzherin, D., Rees, T., et al. (2013). The taxonomic name resolution service: An online tool for automated standardization of plant names. BMC Bioinformatics, 14, 1–14. https://doi.org/10.1186/1471-2105-14-16.
Bridgewater, S., Ratter, J. A., & Felipe Ribeiro, J. (2004). Biogeographic patterns, β-diversity and dominance in the cerrado biome of Brazil. Biodiversity and Conservation, 13, 2295–2318. https://doi.org/10.1023/B:BIOC.0000047903.37608.4c.
Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11, 265–270.
Chao, A., Hsieh, T. C., Chazdon, R. L., Colwell, R. K., & Gotelli, N. J. (2015). Unveiling the species-rank abundance distribution by generalizing the Good-Turing sample coverage theory. Ecology, 96, 1189–1201. https://doi.org/10.1890/14-0550.1.
Coelho, G. A. O., Terra, M. C. N. S., Almeida, H. S., & van den Berg, E. (2016). What can natural edges of gallery forests teach us about woody community performance in sharp ecotones? Journal of Plant Ecology, 10, 937–948. https://doi.org/10.1093/jpe/rtw083.
Comita, L. S., Muller-Landau, H. C., Aguilar, S., & Hubbell, S. P. (2010). Asymmetric density dependence shapes species abundances in a tropical tree community. Science, 329, 330–332. https://doi.org/10.1126/science.1190772.
de Prado, P. I. K. L. (2009). Distribuições de abundâncias de espécies: avanços analíticos para entender um padrão básico em ecologia. Ciência & Ambiente, 1, 121–136.
Eisenlohr, P. V., & Oliveira-Filho, A. T. (2015). Revisiting patterns of tree species composition and their driving forces in the Atlantic forests of Southeastern Brazil. Biotropica. https://doi.org/10.1111/btp.12254.
Fagundes, L. M., de Carvalho, D. A., van den Ber, E., Marques, J. J. G. S., & Machado, E. L. M. (2007). Florística e estrutura do estrato arbóreo de dois fragmentos de florestas decíduas às margens do rio Grande, em Alpinópolis e Passos, MG, Brasil. Acta Bot Brasil, 21, 65–78. https://doi.org/10.1590/s0102-33062007000100007.
Fávero, A. A., Costa, M. D. P., Figueira, M., Andriollo, D. D., & Longhi, S. J. (2015). Distribuição de abundância de espécies da comunidade arbórea do topo de um morro na floresta estacional subtropical. Ciência Rural, 45, 806–813. https://doi.org/10.1590/0103-8478cr20121238.
Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302–4315. https://doi.org/10.1002/joc.5086.
Flather, C. H., & Sieg, C. H. (2001). Species rarity: definition, causes, and classification. In M. G. Raphael & R. Molina (Eds.), Conservation of rare or little-known species: biological, social, and economic considerations (pp. 40–66). Washington: Island Press.
Furniss, T. J., Larson, A. J., & Lutz, J. A. (2017). Reconciling niches and neutrality in a subalpine temperate forest. Ecosphere, 8, e01847. https://doi.org/10.1002/ecs2.1847.
Good, I. J. (1953). The population frequencies of species and the estimation of population parameters. Biometrika, 40, 237–264.
Good, I. J. (2000). Turing’s anticipation of empirical Bayes in connection with the cryptanalysis of the naval enigma. Journal of Statistical Computation and Simulation, 66, 101–111.
Hotelling, H. (1933). Analysis of a complex of statistical variables into principal components. Journal of Educational Psychology, 24, 417–441.
Hubbell, (2013). Tropical rain forest conservation and the twin challenges of diversity and rarity. Ecology and Evolution, 3, 3263–3274.
Hubbell, S. P. (2001). The Unified neutral theory of biodiversity and biogeography. Princeton: Princeton University Press.
Jordano, P. (2016). Sampling networks of ecological interactions. Functional Ecology, 30, 1883–1893. https://doi.org/10.1111/1365-2435.12763.
Kunin, W. E., & Gaston, K. J. (1993). The biology of rarity: patterns, causes and consequences. Trends in Ecology and Evolution, 8, 298–301.
Leitão, R. P., Zuanon, J., Villéger, S., Williams, S. E., Baraloto, C., Fortunel, C., et al. (2016). Rare species contribute disproportionately to the functional structure of species assemblages. Proceedings of the Royal Society B: Biological Sciences, 283, 20160084. https://doi.org/10.1098/rspb.2016.0084.
Lenza, E., Santos, J. O., & Maracahipes-Santos, L. (2015). Species composition, diversity, and vegetation structure in a gallery forest-cerrado sensu stricto transition zone in eastern Mato Grosso, Brazil. Acta Bot Brasil, 29, 327–338. https://doi.org/10.1590/0102-33062014abb3697.
Letcher, S. G., Lasky, J. R., Chazdon, R. L., Norden, N., Wright, S. J., Meave, J. A., et al. (2015). Environmental gradients and the evolution of successional habitat specialization: A test case with 14 Neotropical forest sites. Journal of Ecology, 103, 1276–1290. https://doi.org/10.1111/1365-2745.12435.
Markham, J. (2014). Rare species occupy uncommon niches. Scientific Reports, 4, 63–65. https://doi.org/10.1038/srep06012.
McGill, B. J. (2011). Species abundance distribution. In A. E. Magurran & B. J. McGill (Eds.), Biological diversity: frontiers in measurement and assessment (pp. 105–122). Oxford: Oxford University Press.
McGill, B. J., Etienne, R. S., Gray, J. S., Alonso, D., Anderson, M. J., Benecha, H. K., et al. (2007). Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecology Letters, 10, 995–1015. https://doi.org/10.1111/j.1461-0248.2007.01094.x.
Naves, R. P., Gandolfi, S., & Rother, D. C. (2015). Comparando padrões de distribuição de densidade, diâmetro e abundância de espécies em áreas em processo de restauração. Hoehnea, 42, 737–748. https://doi.org/10.1590/2236-8906-11/rad/2015.
Neeson, T. M., Doran, P. J., Ferris, M. C., Fitzpatrick, K. B., Herbert, M., Khoury, M., et al. (2018). Conserving rare species can have high opportunity costs for common species. Global Change Biology, 24, 3862–3872. https://doi.org/10.1111/gcb.14162.
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D, Minchin PR, O’hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szoecs E, Maintainer HW (2019) Package “vegan” Title Community Ecology Package. https://cran.r-project.org/web/packages/vegan/vegan.pdf. Accessed 25 August 2019
Oliveira-Filho, A. T., & Fontes, M. A. L. (2000). Patterns of floristic differentiation among Atlantic forests in Southeastern Brazil and the influence of climate. Biotropica, 32, 793–810. https://doi.org/10.1111/j.1744-7429.2000.tb00619.x.
Peres-Neto, P. R., Legendre, P., Dray, S., & Borcard, D. (2006). Variation partitioning of species data matrices: Estimation and comparison of fractions. Ecology, 87, 2614–2625.
Pitman, N. C. A., Silman, M. R., & Terborgh, J. W. (2013). Oligarchies in amazonian tree communities: A ten-year review. Ecography, 36, 114–123. https://doi.org/10.1111/j.1600-0587.2012.00083.x.
Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J., & Hirota, M. M. (2009). The Brazilian Atlantic forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142, 1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021.
Rodrigues, A. C., Villa, P. M., & Neri, A. V. (2019). Fine-scale topography shape richness, community composition, stem and biomass hyperdominant species in Brazilian Atlantic forest. Ecological Indicators, 102, 208–217. https://doi.org/10.1016/J.ECOLIND.2019.02.033.
Scolforo, H. F., Scolforo, J. R. S., Mello, C. R., Mello, J. M., & Ferraz Filho, A. C. (2015). Spatial distribution of aboveground carbon stock of the arboreal vegetation in Brazilian biomes of Savanna, Atlantic Forest and semi-arid woodland. PLoS ONE, 10, e0128781. https://doi.org/10.1371/journal.pone.0128781.
Scolforo, J. R. S., & Carvalho, L. M. T. (2006). Mapeamento e inventário da flora nativa e dos reflorestamentos de Minas Gerais. Lavras: Editora UFLA.
Scott, W. A., & Hallam, C. J. (2003). Assessing species misidentification rates through quality assurance of vegetation monitoring. Pl Ecol, 165, 101–115. https://doi.org/10.1023/A:1021441331839.
Silva, I. A., Cianciaruso, M. V., & Batalha, M. A. (2010). Abundance distribution of common and rare plant species of Brazilian savannas along a seasonality gradient. Acta Bot Brasil, 24, 407–413. https://doi.org/10.1590/S0102-33062010000200011.
Silveira, E. M. O., Cunha, L. I. F., Galvão, L. S., Withey, K. D., Acerbi Júnior, F. W., & Scolforo, J. R. S. (2019d). Modelling aboveground biomass in forest remnants of the Brazilian Atlantic Forest using remote sensing, environmental and terrain-related data. Geocarto International. https://doi.org/10.1080/10106049.2019.1594394.
Silveira, E. M. O., Espírito-Santo, F., Wulder, M. A., Acerbi-Junior, F. W., Carvalho, M. C., Mello, C. R., et al. (2019a). Pre-stratified modelling plus residuals kriging reduces the uncertainty of aboveground biomass estimation and spatial distribution in heterogeneous savannas and forest environments. Forest Ecology and Management, 445, 96–109. https://doi.org/10.1016/j.foreco.2019.05.016.
Silveira, E. M. O., Silva, S. H. G., Acerbi-junior, F. W., Carvalho, M. C., Carvalho, L. M. T., Scolforo, J. R. S., et al. (2019b). Object-based random forest modelling of aboveground forest biomass outperforms a pixel-based approach in a heterogeneous and mountain tropical environment. International Journal of Applied Earth Observation Geoinformation, 78, 175–188. https://doi.org/10.1016/j.jag.2019.02.004.
Silveira, E. M. O., Terra, M. C. N. S., Acerbi-Júnior, F. W., & Scolforo, J. R. S. (2019c). Estimating aboveground biomass loss from deforestation in the savanna and semi-arid biomes of Brazil between 2007 and 2017. In M. N. Suratman, Z. A. Latif, G. de Oliveira, N. Brunsell, Y. Shimabukuro, & C. A. C. dos Santos (Eds.), Tropical forests in transition—the role of deforestation and impacts from community composition to regional climate change (pp. 1–17). London: IntechOpen. https://doi.org/10.5772/intechopen.85660.
Slik, J. W. F., Arroyo-Rodríguez, V., Aiba, S.-I., et al. (2015). An estimate of the number of tropical tree species. Proceedings of National Academy of Science USA, 112, 7472–7477. https://doi.org/10.1073/pnas.1423147112.
Tabarelli, M., Peres, C. A., & Melo, F. P. L. (2012). The “few winners and many losers” paradigm revisited: Emerging prospects for tropical forest biodiversity. Biological Conservation, 155, 136–140. https://doi.org/10.1016/j.biocon.2012.06.020.
ter Steege, H., Pitman, N. C., Sabatier, D., et al. (2013). Hyperdominance in the Amazonian tree flora. Science, 342, 1243092. https://doi.org/10.1126/science.1243092.
Terra, M. C. N. S., dos Santos, R. M., Fontes, M. A. L., de Mello, J. M., Scolforo, J. R. S., Gomide, L. R., et al. (2017). Tree dominance and diversity in Minas Gerais, Brazil. Biodiversity and Conservation, 26, 2133–2153. https://doi.org/10.1007/s10531-017-1349-1.
Terra, M. C. N. S., Mello, J. M., Mello, C. R., Santos, R. M., Nunes, A. C. R., & Raimundo, M. R. (2015). Influência topo-edafo-climática na vegetação de um fragmento de Mata Atlântica na Serra da Mantiqueira, MG. Ambiagua, 10, 928–942. https://doi.org/10.4136/ambi-agua.1705.
Terra, M. C. N. S., Santos, R. M., Prado Júnior, J. A., Mello, J. M., Scolforo, J. R. S., Fontes, M. A. L., et al. (2018). Water availability drives gradients of tree diversity, structure and functional traits in the Atlantic-Cerrado-Caatinga transition, Brazil. Journal of Plant Ecology, 11, 803–814. https://doi.org/10.1093/jpe/rty017.
Tokeshi, M. (1990). Niche apportionment or random assortment: Species abundance patterns revisited. Journal of Animal Ecology, 59, 1129–1146. https://doi.org/10.2307/5036.
Tovo, A., Suweis, S., Formentin, M., Favretti, M., Volkov, I., Banavar, J. R., et al. (2017). Upscaling species richness and abundances in tropical forests. Science Advances, 3, e1701438. https://doi.org/10.1126/sciadv.1701438.
Villa, P. M., Martins, S. V., Rodrigues, A. C., Safar, N. V. H., Bonilla, M. A. C., & Ali, A. (2019). Testing species abundance distribution models in tropical forest successions: Implications for fine-scale passive restoration. Ecological Engineering, 135, 28–35. https://doi.org/10.1016/j.ecoleng.2019.05.015.
Wang, Q., Su, X., Shrestha, N., Liu, Y., Wang, S., Xu, X., et al. (2017). Historical factors shaped species diversity and composition of Salix in eastern Asia. Scientific Reports, 7, 1–10. https://doi.org/10.1038/srep42038.
Wilson, J. B. (2011). The twelve theories of co-existence in plant communities: the doubtful, the important and the unexplored. Journal of Vegetation Science, 22, 184–195.
Zhang, J., Qiao, X., Liu, Y., Lu, J., Jiang, M., Tang, Z., et al. (2015). Species-abundance distributions of tree species varies along climatic gradients in China’s forests. Journal of Plant Ecology, 9, 240. https://doi.org/10.1093/jpe/rtv055.
Acknowledgements
The first author would like to thank the Programa de Pós-Graduação em Engenharia Florestal (Universidade Federal de Lavras) for the postdoc position opportunity. This study was supported in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.
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This study was supported in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance Code 001.
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Terra, M.d.C.N.S., Silveira, E.M.d.O., Withey, K.D. et al. Unseen rare tree species in southeast Brazilian forests: a species abundance distribution approach. COMMUNITY ECOLOGY 21, 229–238 (2020). https://doi.org/10.1007/s42974-020-00025-4
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DOI: https://doi.org/10.1007/s42974-020-00025-4