Combining ecological niche models with experimental seed germination to estimate the effect of climate change on the distribution of endangered plant species in the Brazilian Cerrado

Springer Science and Business Media LLC - Tập 194 - Trang 1-15 - 2022
Rafael Batista Ferreira1,2, Micael Rosa Parreira3, Filipe Viegas de Arruda1,4, Marcus J. A. Falcão5, Vidal de Freitas Mansano5, João Carlos Nabout1
1Universidade Estadual de Goiás, Fazenda Barreiro Do Meio, Anápolis, Goiás, Brazil
2Faculdade Metropolitana de Anápolis, Anápolis, Goiás, Brazil
3Universidade Federal de Goiás, Chácaras de Recreio Samambaia, Goiânia, Goiás, Brazil
4Instituto de Pesquisa Ambiental da Amazônia, Brasília, Brazil
5Instituto de Pesquisas Jardim Botânico Do Rio de Janeiro, DIPEQ. Rua Pacheco Leão 915, Rio de Janeiro, Brazil

Tóm tắt

Predicting the geographic distribution of plants that provide ecosystem services is essential to understand the adaptation of communities and conserve that group toward climate change. Predictions can be more accurate if changes in physiological characteristics of species due to those changes are included. Thus, we aimed to evaluate the impacts of climate change on the different hierarchical levels of Apuleia leiocarpa (Vogel) J. F. Macbr. (Fabaceae). Therefore, we experimentally evaluate the effect of different temperatures on the initial development (vigor) and estimate the impact of climate change on the potential geographic distribution of the species, using ecological niche approaches. For the experiment, we used 11 temperature intervals of 2 °C ranging from 21 to 41 °C. We used ecological niche modeling techniques (ENM) to predict the species’ environmental suitability in future climate scenarios. The association between the experiment and niche models was obtained by testing the relationships of temperature increase on the species vigor and geographic distribution. This conceptual model to determine the direct and indirect effects of temperature was generated using the methodological framework of structural equation models. The experiment showed that the seeds had the highest growth at 31 °C. ENMs indicated that due to climate change, there is a tendency for the plant to migrate to regions with milder temperatures. However, such regions may be unsuitable for the plant since they do not have ideal temperatures to germinate, which may cause a drastic reduction in their availability in a future climate change scenario. The inclusion of seed germination through experimental research allowed us to detect an area that is less suitable for germination despite being climatically suitable for the species. Thus, research that integrates the effect of climate on the different stages of the organism’s development is essential to understand the impact of climate change on biodiversity.

Tài liệu tham khảo

Agostini, V. O., Macedo, A. J., Muxagata, E., da Silva, M. V., & Pinho, G. L. L. (2019). Natural and non-toxic products from Fabaceae Brazilian plants as a replacement for traditional antifouling biocides: An inhibition potential against initial biofouling. Environmental Science and Pollution Research, 26(26), 27112–27127. https://doi.org/10.1007/s11356-019-05744-4 Alarcón, D., & Cavieres, L. A. (2018). Relationships between ecological niche and expected shifts in elevation and latitude due to climate change in South American temperate forest plants. Journal of Biogeography, 45(10), 2272–2287. https://doi.org/10.1111/jbi.13377 Almeida, S. D., Proença, C. E., Sano, S. M., & Ribeiro, J. F. (1998). Cerrado: espécies vegetais úteis. Planaltina: EMBRAPA-CPAC. Araújo, M. B., & Peterson, A. T. (2012). Uses and misuses of bioclimatic envelope modeling. Ecology, 93(7), 1527–1539. https://doi.org/10.1890/11-1930.1 Barbet-Massin, M., Jiguet, F., Albert, C. H., & Thuiller, W. (2012). Selecting pseudo-absences for species distribution models: How, where and how many? Methods in Ecology and Evolution, 3(2), 327–338. https://doi.org/10.1111/j.2041-210X.2011.00172.x Barve, N., Barve, V., Jiménez-Valverde, A., Lira-Noriega, A., Maher, S. P., Peterson, A. T., et al. (2011). The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling, 222(11), 1810–1819. https://doi.org/10.1016/j.ecolmodel.2011.02.011 Bentler, P. M. (1990). Comparative fit indexes in structural models. Psychological Bulletin, 107(2), 238–246. https://doi.org/10.1037/0033-2909.107.2.238 Bewley, J. D., Bradford, K. J., Hilhorst, H. W. M., & Nonogaki, H. (2013). Seeds: Physiology of development, germination and dormancy (3rd ed.). New York, NY: Springer New York. https://doi.org/10.1007/978-1-4614-4693-4 Burnham, K. P., & Anderson, D. R. (2002). Model selection and multi-model inference: A practical information-theoretic approach. Springer-Verlag. Carbognani, M., Tomaselli, M., & Petraglia, A. (2018). Different temperature perception in high-elevation plants: New insight into phenological development and implications for climate change in the alpine tundra. Oikos, 127(7), 1014–1023. https://doi.org/10.1111/oik.04908 Carpenter, G., Gillison, A. N., & Winter, J. (1993). Domain - A flexible modeling procedure for mapping potential distributions of plants and animals. Biodiversity and Conservation, 2(6), 667–680. https://doi.org/10.1007/BF00051966 Collevatti, R. G., Nabout, J. C., & Diniz-Filho, J. A. F. (2011). Range shift and loss of genetic diversity under climate change in Caryocar brasiliense, a Neotropical tree species. Tree Genetics & Genomes, 7(6), 1237–1247. https://doi.org/10.1007/s11295-011-0409-z da Cunha, H. F., Ferreira, É. D., Tessarolo, G., & Nabout, J. C. (2018). Host plant distributions and climate interact to affect the predicted geographic distribution of a Neotropical termite. Biotropica, 50(4), 625–632. https://doi.org/10.1111/btp.12555 de Carvalho, A., S., da Silva, M. V., Gomes, F. S., Paiva, P. M. G., Malafaia, C. B., da Silva, T. D., et al. (2015). Purification, characterization and antibacterial potential of a lectin isolated from Apuleia leiocarpa seeds. International Journal of Biological Macromolecules, 75, 402–408. https://doi.org/10.1016/j.ijbiomac.2015.02.001 de Oliveira, G., de Souza Barreto, B., & da Silva dos Santos, D., Queiroz de Matos, V., & Seara Santos, M. C. (2018). Combining the effects of biological invasion and climate change into systematic conservation planning for the Atlantic Forest. Biological Invasions, 20(10), 2753–2765. https://doi.org/10.1007/s10530-018-1727-y de Oliveira, G., Lima-Ribeiro, M. S., Terribile, L. C., Dobrovolski, R., Telles, M. P., & d. C., & Diniz-Filho, J. A. F. (2015). Conservation biogeography of the Cerrado’s wild edible plants under climate change: Linking biotic stability with agricultural expansion. American Journal of Botany, 102(6), 870–877. https://doi.org/10.3732/ajb.1400352 de Siqueira, M. F., & Peterson, A. T. (2003). Consequences of global climate change for geographic distributions of cerrado tree species. Biota Neotropica, 3(2), 1–14. https://doi.org/10.1590/S1676-06032003000200005 Donat, M. G., & Alexander, L. V. (2012). The shifting probability distribution of global daytime and night-time temperatures. Geophysical Research Letters, 39(14). https://doi.org/10.1029/2012GL052459 Duputié, A., Rutschmann, A., Ronce, O., & Chuine, I. (2015). Phenological plasticity will not help all species adapt to climate change. Global Change Biology, 21(8), 3062–3073. https://doi.org/10.1111/gcb.12914 Fan, Y., Chen, J., Shirkey, G., John, R., Wu, S. R., Park, H., & Shao, C. (2016). Applications of structural equation modeling (SEM) in ecological studies: An updated review. Ecological Processes, 5(1), 19. https://doi.org/10.1186/s13717-016-0063-3 Fei, S., Desprez, J. M., Potter, K. M., Jo, I., Knott, J. A., & Oswalt, C. M. (2017). Divergence of species responses to climate change. Science Advances, 3(5). https://doi.org/10.1126/sciadv.1603055 Ferreira, R. B., Parreira, M. R., & Nabout, J. C. (2021). The impact of global climate change on the number and replacement of provisioning ecosystem services of Brazilian Cerrado plants. Environmental Monitoring and Assessment, 193(11), 731. https://doi.org/10.1007/s10661-021-09529-6 Francon, L., Corona, C., Till-Bottraud, I., Carlson, B. Z., & Stoffel, M. (2020). Some (do not) like it hot: Shrub growth is hampered by heat and drought at the alpine treeline in recent decades. American Journal of Botany, 107(4), 607–617. https://doi.org/10.1002/ajb2.1459 GBIF.org. (2019). GBIF Occurrence Download. https://doi.org/10.15468/dl.h29da5 Gonçalves, T. V., de Gomes, M. A., & A., & Nabout, J. C. (2020). The historical geography, bioclimatic, and informetric conditions of protected areas in the Brazilian Cerrado. Journal for Nature Conservation, 58, 125905. https://doi.org/10.1016/j.jnc.2020.125905 Hannah, L., Midgley, G. F., & Millar, D. (2002). Climate change-integrated conservation strategies. Global Ecology and Biogeography, 11(6), 485–495. https://doi.org/10.1046/j.1466-822X.2002.00306.x Heinicka, G. D. S., Braga, L. F., Sousa, M. P., & Carvalho, M. A. C. (2006). Germinação de sementes de Apuleia leiocarpa (Vogel.) JF Macbr.: temperatura, fotoblastismo e estresse salino. Revista de Ciências Agro-Ambientais, 4(1), 37–46. Hengl, T., Mendes de Jesus, J., Heuvelink, G. B. M., Ruiperez Gonzalez, M., Kilibarda, M., Blagotić, A., et al. (2017). SoilGrids250m: Global gridded soil information based on machine learning. PLoS One, 12(2), e0169748. https://doi.org/10.1371/journal.pone.0169748 Hernández-Stefanoni, J. L., Gallardo-Cruz, J. A., Meave, J. A., & Dupuy, J. M. (2011). Combining geostatistical models and remotely sensed data to improve tropical tree richness mapping. Ecological Indicators, 11(5), 1046–1056. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25(15), 1965–1978. https://doi.org/10.1002/joc.1276 Hu, L., & Bentler, P. M. (1999). Cutoff criteria for fit indexes in covariance structure analysis: Conventional criteria versus new alternatives. Structural Equation Modeling: A Multidisciplinary Journal, 6(1), 1–55. https://doi.org/10.1080/10705519909540118 Hughes, T. P., Kerry, J. T., Baird, A. H., Connolly, S. R., Chase, T. J., Dietzel, A., et al. (2019). Global warming impairs stock–recruitment dynamics of corals. Nature, 568(7752), 387–390. https://doi.org/10.1038/s41586-019-1081-y Kearney, M., & Porter, W. (2009). Mechanistic niche modelling: Combining physiological and spatial data to predict species’ ranges. Ecology Letters, 12(4), 334–350. Koutsovoulou, K., Daws, M. I., & Thanos, C. A. (2014). Campanulaceae: A family with small seeds that require light for germination. Annals of Botany, 113(1), 135–143. https://doi.org/10.1093/aob/mct250 Li, C., Yu, F., Li, Y., Niu, W., Li, J., Yang, J., & Liu, K. (2020). Comparative analysis of the seed germination of pakchoi and its phytoremediation efficacy combined with chemical amendment in four polluted soils. International Journal of Phytoremediation, 22(11), 1156–1167. https://doi.org/10.1080/15226514.2020.1741508 Marques, A. R., Atman, A. P. F., Silveira, F. A. O., & de Lemos-Filho, J. P. (2014). Are seed germination and ecological breadth associated? Testing the regeneration niche hypothesis with bromeliads in a heterogeneous neotropical montane vegetation. Plant Ecology, 215(5), 517–529. https://doi.org/10.1007/s11258-014-0320-4 Martinelli, G., & Moraes, M. A. (2013). Livro Vermelho da Flora do Brasil. (Andrea Jakobsson, Ed.). Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. http://dspace.jbrj.gov.br/jspui/handle/doc/26 (Accessed 14 Dec 2021) McLean, N., Lawson, C. R., Leech, D. I., & Pol, M. (2016). Predicting when climate-driven phenotypic change affects population dynamics. Ecology Letters, 19(6), 595–608. https://doi.org/10.1111/ele.12599 Medeiros, J. A. D. D., Nunes, S. P. L., Félix, F. C., Ferrari, C. D. S., Pacheco, M. V., & Torres, S. B. (2020). Vigor test of (strong) normal intact Amburana cearensis (Allemão) AC Smith seedlings. Journal of Seed Science, 42. Nabout, J. C., Caetano, J. M., Ferreira, R. B., Teixeira, I. R., & Alves, S. D. F. (2012). Using correlative, mechanistic and hybrid niche models to predict the productivity and impact of global climate change on maize crop in Brazil. Nature Conservation, 10(2), 177–183. Nabout, J. C., Magalhães, M. R., de Amorim Gomes, M. A., & da Cunha, H. F. (2016). The impact of global climate change on the geographic distribution and sustainable harvest of Hancornia speciosa Gomes (Apocynaceae) in Brazil. Environmental Management, 57(4), 814–821. https://doi.org/10.1007/s00267-016-0659-5 Nabout, J. C., Oliveira, G., Magalhães, M. R., Carina, T. L., & de Almeida, F. A. S. (2011). Global climate change and the production of Pequi fruits (Caryocar brasiliense) in the Brazilian Cerrado. Natureza & Conservação, 9(1), 55–60. https://doi.org/10.4322/natcon.2011.006 Nabout, J. C., Soares, T., Diniz-Filho, J., De Marco Júnior, P., Telles, M., Naves, R., & Chaves, L. (2010). Combining multiple models to predict the geographical distribution of the Baru tree (Dipteryx alata Vogel) in the Brazilian Cerrado. Brazilian Journal of Biology, 70(4), 911–919. https://doi.org/10.1590/S1519-69842010000500001 Nelder, J. A., & Wedderburn, R. W. M. (1972). Generalized linear models. Journal of the Royal Statistical Society. Series A (General), 135(3), 370–384. https://doi.org/10.2307/2344614 Newbold, T., Hudson, L. N., Hill, S. L. L., Contu, S., Lysenko, I., Senior, R. A., et al. (2015). Global effects of land use on local terrestrial biodiversity. Nature, 520(7545), 45–50. https://doi.org/10.1038/nature14324 Niu, Y., Yang, S., Zhou, J., Chu, B., Ma, S., Zhu, H., & Hua, L. (2019). Vegetation distribution along mountain environmental gradient predicts shifts in plant community response to climate change in alpine meadow on the Tibetan Plateau. Science of the Total Environment, 650, 505–514. https://doi.org/10.1016/j.scitotenv.2018.08.390 Nix, H. A. (1986). A biogeographic analysis of Australian elapid snakes. In Atlas of elapid snakes of Australia, 7, 4–15. Canberra: Australian Government Publishing Service. Padilha, M. S., Sobral, L. S., Baretta, C. R. D. M., & de Abreu, L. (2018). Substratos e teor de umidade para o teste de germinação de sementes de Apuleia leiocarpa (Vog.) Macbr. Revista Verde de Agroecologia e Desenvolvimento Sustentável, 13(4), 437–444. Parmesan, C., & Hanley, M. E. (2015). Plants and climate change: Complexities and surprises. Annals of Botany, 116(6), 849–864. https://doi.org/10.1093/aob/mcv169 Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190(3–4), 231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026 Porceddu, M., Mattana, E., Pritchard, H. W., & Bacchetta, G. (2013). Thermal niche for in situ seed germination by Mediterranean mountain streams: Model prediction and validation for Rhamnus persicifolia seeds. Annals of Botany, 112(9), 1887–1897. https://doi.org/10.1093/aob/mct238 R Core Team. (2019). A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. https://www.r-project.org/ Reed, T. E., Schindler, D. E., Waples, R. S., Reed, T. E., Schindler, D. E., & Waples, R. S. (2011). Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conservation Biology, 25(1), 56–63. https://doi.org/10.1111/j.1523-1739.2010.01552.x Revelle, W. (2019). Psych: Procedures for personality and psychological research. Evanston, Illinois, USA: Northwestern University. https://cran.r-project.org/package=psych Ribeiro, R. M., Tessarolo, G., Soares, T. N., Teixeira, I. R., & Nabout, J. C. (2019). Global warming decreases the morphological traits of germination and environmental suitability of Dipteryx alata (Fabaceae) in Brazilian Cerrado. Acta Botanica Brasilica, 33(3), 446–453. https://doi.org/10.1590/0102-33062018abb0288 Rosseel, Y. (2012). lavaan : An R package for structural equation modeling. Journal of Statistical Software, 48(2), 1–36. https://doi.org/10.18637/jss.v048.i02 Saha, S., Chakraborty, D., Sehgal, V. K., & Pal, M. (2015). Rising atmospheric CO2: Potential impacts on chickpea seed quality. Agriculture, Ecosystems & Environment, 203, 140–146. https://doi.org/10.1016/j.agee.2015.02.002 Sano, E. E., Rodrigues, A. A., Martins, E. S., Bettiol, G. M., Bustamante, M. M. C., Bezerra, A. S., et al. (2019). Cerrado ecoregions: A spatial framework to assess and prioritize Brazilian savanna environmental diversity for conservation. Journal of Environmental Management, 232, 818–828. https://doi.org/10.1016/j.jenvman.2018.11.108 Sato, M., Nanami, A., Bayne, C. J., Makino, M., & Hori, M. (2020). Changes in the potential stocks of coral reef ecosystem services following coral bleaching in Sekisei Lagoon, southern Japan: Implications for the future under global warming. Sustainability Science, 15(3), 863–883. https://doi.org/10.1007/s11625-019-00778-6 Schölkopf, B., Platt, J. C., Shawe-Taylor, J., Smola, A. J., & Williamson, R. C. (2001). Estimating the support of a high-dimensional distribution. Neural Computation, 13(7), 1443–1471. https://doi.org/10.1162/089976601750264965 Simon, L. M., de Oliveira, G., de Barreto, B., & S., Nabout, J. C., Rangel, T. F. L. V. B., & Diniz-Filho, J. A. F. (2013). Effects of global climate changes on geographical distribution patterns of economically important plant species in cerrado. Revista Árvore, 37(2), 267–274. https://doi.org/10.1590/S0100-67622013000200008 Solarik, K. A., Messier, C., Ouimet, R., Bergeron, Y., & Gravel, D. (2018). Local adaptation of trees at the range margins impacts range shifts in the face of climate change. Global Ecology and Biogeography, 27(12), 1507–1519. https://doi.org/10.1111/geb.12829 Strassburg, B. B. N., Brooks, T., Feltran-Barbieri, R., Iribarrem, A., Crouzeilles, R., Loyola, R., et al. (2017). Moment of truth for the Cerrado hotspot. Nature Ecology & Evolution, 1(4), 0099. https://doi.org/10.1038/s41559-017-0099 Sousa, F. D. P. S., Lewis, G. P., & Hawkins, J. A. (2010). A revision of the South American genus Apuleia (Leguminosae, Cassieae). Kew Bulletin, 65(2), 225–232. Swets, J. (1988). Measuring the accuracy of diagnostic systems. Science, 240(4857), 1285–1293. https://doi.org/10.1126/science.3287615 Tambosi, L. R., Martensen, A. C., Ribeiro, M. C., & Metzger, J. P. (2014). A framework to optimize biodiversity restoration efforts based on habitat amount and landscape connectivity. Restoration Ecology, 22(2), 169–177. https://doi.org/10.1111/rec.12049 The Intergovernmental Panel On Climate Change (IPCC). (2021). The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Masson-Delmotte, V., Zhai P., Pirani A., Connors S.L., Péan C., Berger S., et al. (eds.). Cambridge University Press. In Press. Turchetto, F., Araujo, M. M., Callegaro, R. M., Griebeler, A. M., Mezzomo, J. C., Berghetti, Á. L. P., & Rorato, D. G. (2017). Phytosociology as a tool for forest restoration: A study case in the extreme South of Atlantic Forest Biome. Biodiversity and Conservation, 26(6), 1463–1480. https://doi.org/10.1007/s10531-017-1310-3 Valladares, F., Matesanz, S., Guilhaumon, F., Araújo, M. B., Balaguer, L., Benito-Garzón, M., et al. (2014). The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecology Letters, 17(11), 1351–1364. https://doi.org/10.1111/ele.12348 Vaz, Ú. L., & Nabout, J. C. (2016). Using ecological niche models to predict the impact of global climate change on the geographical distribution and productivity of Euterpe oleracea Mart. (Arecaceae) in the Amazon. Acta Botanica Brasilica, 30(2). https://doi.org/10.1590/0102-33062016abb0036 Velazco, S. J. E., Galvão, F., Villalobos, F., & De Marco Júnior, P. (2017). Using worldwide edaphic data to model plant species niches: An assessment at a continental extent. PLoS One, 12(10), e0186025. https://doi.org/10.1371/journal.pone.0186025 Velazco, S. J. E., Villalobos, F., Galvão, F., & De Marco Júnior, P. (2019). A dark scenario for Cerrado plant species: Effects of future climate, land use and protected areas ineffectiveness. Diversity and Distributions, 25(4), 660–673. https://doi.org/10.1111/ddi.12886 Villén-Peréz, S., Heikkinen, J., Salemaa, M., & Mäkipää, R. (2020). Global warming will affect the maximum potential abundance of boreal plant species. Ecography, 43(6), 801–811. https://doi.org/10.1111/ecog.04720 Walck, J. L., Hidayati, S. N., Dixon, K. W., Thompson, K., & Poschlod, P. (2011). Climate change and plant regeneration from seed. Global Change Biology, 17(6), 2145–2161. https://doi.org/10.1111/j.1365-2486.2010.02368.x Wang, C., Xiao, H., Zhao, L., Liu, J., Wang, L., Zhang, F., et al. (2016). The allelopathic effects of invasive plant Solidago canadensis on seed germination and growth of Lactuca sativa enhanced by different types of acid deposition. Ecotoxicology, 25(3), 555–562. https://doi.org/10.1007/s10646-016-1614-1 Warren, R., Price, J., Graham, E., Forstenhaeusler, N., & VanDerWal, J. (2018). The projected effect on insects, vertebrates, and plants of limiting global warming to 1.5 °C rather than 2 °C. Science, 360(6390), 791–795. https://doi.org/10.1126/science.aar3646 Wiens, J. J., Ackerly, D. D., Allen, A. P., Anacker, B. L., Buckley, L. B., Cornell, H. V., et al. (2010). Niche conservatism as an emerging principle in ecology and conservation biology. Ecology Letters, 13(10), 1310–1324. https://doi.org/10.1111/j.1461-0248.2010.01515.x Wisz, M. S., Pottier, J., Kissling, W. D., Pellissier, L., Lenoir, J., Damgaard, C. F., et al. (2013). The role of biotic interactions in shaping distributions and realised assemblages of species: Implications for species distribution modeling. Biological Reviews, 88(1), 15–30. https://doi.org/10.1111/j.1469-185X.2012.00235.x