Abstract
The impacts of invasive alien species are determined by their abundance, a relationship that usually does not follow linear trends owing to the complexity of ecological interactions. Abundance-impact curves are essential for informing evidence-based management interventions because they can reveal how per-capita impact changes as the invader become more abundant. Across 12 invasion gradients occurring in two areas, we constructed abundance-impact curves for the invasive grass Urochloa decumbens in a tropical savanna (Cerrado). We used generalized additive models to assess how increases in the invader’s abundance influenced system properties from the microhabitat to ecosystem levels. At the microhabitat level, increasing invader abundance resulted in nonlinear effects on bare soil and illuminance but a linear reduction in temperature fluctuations. The specific leaf area of dominant plants linearly increased with invader abundance. We found higher per-capita effects of Urochloa decumbens on the native graminoid cover when the invader was at low levels of abundance. Conversely, the per-capita effects on native species richness were higher at moderate levels of invasion. These results indicate the immediate impacts of the invader on the abundance of functionally similar native grasses but greater impacts on species richness only at moderate levels of invasion. The total biomass increased through the invasion gradient. Despite these changes, the abundance of invasive species did not influence the ecosystem properties. Our findings support the functional redundancy between Urochloa decumbens and native dominant grasses; however, despite this similarity, Urochloa decumbens promotes negative impacts at the microhabitat, organism, and community levels.
Resumo
O impacto de plantas exóticas invasoras é determinado por sua abundância, uma relação que geralmente não tem padrões lineares devido à complexidade das interações ecológicas. Curvas de abundância-impacto são essenciais para informar ações de manejo, já que revelam como os impactos per-capita da invasora mudam à medida que a espécie se torna mais abundante. Ao longo de 12 gradientes de invasão localizados em duas áreas, nós construímos curvas de abundância-impacto da gramínea invasora Urochloa decumbens em uma savana tropical (Cerrado). Nós utilizamos modelos aditivos generalizados para investigar como a abundância da invasora influencia propriedades do sistema invadido, desde o nível de micro-habitat até o nível de ecossistema. O aumento da abundância da invasora resultou em efeitos não lineares sobre a porcentagem de solo nu e na iluminância a nível do solo, mas em uma redução linear na flutuação de temperatura do ar. A área foliar específica a nível de comunidade acompanhou o aumento na abundância da invasora. Encontramos um maior efeito per-capita de Urochloa decumbens na cobertura por gramíneas nativas em baixos níveis de abundância da invasora. Contrariamente, os efeitos per-capita na riqueza de espécies nativas foram maiores em níveis moderados de invasão. Estes resultados indicam efeitos imediatos da invasora na abundância de espécies funcionalmente similares de gramíneas, porém impactos mais pronunciados na riqueza de espécies somente em níveis intermediários de invasão. A biomassa total aumentou ao longo do gradiente de invasão devido ao aumento de biomassa da invasora. Esses resultados suportam uma redundância funcional entre Urochloa decumbens e gramíneas nativas, mas demonstram também os impactos negativos da invasora nos níveis de micro-habitat, indivíduos e comunidades.
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References
Al-Tam F, Adam H, Dos Anjos A et al (2013) P-TRAP: a panicle trait phenotyping tool. BMC Plant Biol 13:122
Almeida-Neto M, Prado PI, Kubota U et al (2010) Invasive grasses and native Asteraceae in the Brazilian Cerrado. Plant Ecol 209:109–122. https://doi.org/10.1007/s11258-010-9727-8
Almeida S, Louzada J, Sperber C, Barlow J (2011) Subtle land-use change and tropical biodiversity: dung beetle communities in cerrado grasslands and exotic pastures. Biotropica 43:704–710
Assis GB de (2017) Invasão do campo cerrado por braquiária (Urochloa decumbens): perdas de diversidade e experimentação de técnicas de restauração. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro
Assis GB, Pilon NAL, Siqueira MF, Durigan G (2021) Effectiveness and costs of invasive species control using different techniques to restore cerrado grasslands. Restor Ecol 29:1. https://doi.org/10.1111/rec.13219
Augustine DJ (2003) Spatial heterogeneity in the herbaceous layer of a semi-arid savanna ecosystem. Plant Ecol 167:319
Barbosa EG, Pivello VR, Meirelles ST (2008) Allelopathic evidence in Brachiaria decumbens and its potential to invade the Brazilian cerrados. Brazilian Arch Biol Technol 51:825–831. https://doi.org/10.1590/S1516-89132008000400021
Baruch Z, Hernandez AB, Montilla M (1989) Dinamica del crecimiento, fenologia y reparticion de biomasa gramineas nativas e introducidas de una sabana neotropical. Ecotropicos 2:1–13
Batten KM, Scow KM, Espeland EK (2008) Soil microbial community associated with an invasive grass differentially impacts native plant performance. Microb Ecol 55:220–228. https://doi.org/10.1007/s00248-007-9269-3
Bond WJ, Parr CL (2010) Beyond the forest edge: Ecology, diversity and conservation of the grassy biomes. Biol Conserv 143:2395–2404. https://doi.org/10.1016/j.biocon.2009.12.012
Bradford MA, Jones TH, Bardgett RD et al (2002) Impacts of soil faunal community composition on model grassland ecosystems. Science 298:615–618. https://doi.org/10.1126/science.1075805
Bradley BA, Laginhas BB, Whitlock R et al (2019) Disentangling the abundance–impact relationship for invasive species. Proc Natl Acad Sci USA 116:9919–9924. https://doi.org/10.1073/pnas.1818081116
Brando PM, Durigan G (2004) Changes in cerrado vegetation after disturbance by frost (São Paulo State, Brazil). Plant Ecol 175:205–215
Brooks KJ, Setterfield SA, Douglas MM (2010) Exotic grass invasions: Applying a conceptual framework to the dynamics of degradation and restoration in Australia’s tropical savannas. Restor Ecol 18:188–197. https://doi.org/10.1111/j.1526-100X.2008.00470.x
Brossard M, Barcellos ADO (2005) Conversão do Cerrado em pastagense cultivadas e funcionamento de latossolos. Cad Ciência e Tecnol 22:153–168
Castro-Díez P, Pauchard A, Traveset A, Vilà M (2016) Linking the impacts of plant invasion on community functional structure and ecosystem properties. J Veg Sci 27:1233–1242. https://doi.org/10.1111/jvs.12429
Chong KY, Corlett RT, Nuñez MA et al (2021) Are terrestrial biological invasions different in the tropics? Annu Rev Ecol Evol Syst 52:1. https://doi.org/10.1146/annurev-ecolsys-012021-095454
Coleman HM, Levine JM (2007) Mechanisms underlying the impacts of exotic annual grasses in a coastal California meadow. Biol Invasions 9:65–71. https://doi.org/10.1007/s10530-006-9008-6
D’Odorico P, Laio F, Ridolfi L (2006) A probabilistic analysis of fire-induced tree-grass coexistence in savannas. Am Nat 167:E79–E87. https://doi.org/10.1086/500617
Dairel M, Fidelis A (2020) The presence of invasive grasses affects the soil seed bank composition and dynamics of both invaded and non-invaded areas of open savannas. J Environ Manag 276:111291. https://doi.org/10.1016/j.jenvman.2020.111291
Damasceno G, Fidelis A (2020) Abundance of invasive grasses is dependent on fire regime and climatic conditions in tropical savannas. J Environ Manage 271:111016. https://doi.org/10.1016/j.jenvman.2020.111016
Damasceno G, Souza L, Pivello VRVR et al (2018) Impact of invasive grasses on Cerrado under natural regeneration. Biol Invasions. https://doi.org/10.1007/s10530-018-1800-6
Damasceno G, Fidelis A (2023) Plant biodiversity and associated environmental data for a tropical savanna following invasion by Urochloa decumbens, Cerrado region, Brazil, 2019–2021. Environ Inform Data Centre. https://doi.org/10.5285/abcabfe2-612c-4cab-b626-641002fc442e
Damgaard C (2014) Quantitative plant ecology: Statistical and ecological modelling of plant abundance. E-book
de Queiroz ACM, Rabello AM, Braga DL et al (2020) Cerrado vegetation types determine how land use impacts ant biodiversity. Biodivers Conserv 29:2017–2034
Diagne C, Leroy B, Vaissière A-C et al (2021) High and rising economic costs of biological invasions worldwide. Nature. https://doi.org/10.1038/s41586-021-03405-6
Dias-Filho MB (1983) Limitações e potencial de Brachiaria humidicola para o trópico úmido brasileiro. Embrapa, Belém
Dias-Filho MB (2000) Growth and biomass allocation of the C 4 Grasses Brachiaria Brizantha and B. Humidicola under Shade Pesqui Agropecuária Bras 3512:2335–2341
Douglas MM, Setterfield SA, Rossiter N, et al (2004) Effects of mission grass (Pennisetum polystachion ( L.) Schult.) invasion on fuel loads and nitrogen availability in a northern Australia tropical savanna. Fourteenth Aust Weeds Conf 179–181
Drenovsky RE, Batten KM (2007) Invasion by Aegilops triuncialis (barb goatgrass) slows carbon and nutrient cycling in a serpentine grassland. Biol Invasions 9:107–116. https://doi.org/10.1007/s10530-006-0007-4
Evans RD, Rimer R, Sperry L, Belnap J (2001) Exotic plant invasion alters nitrogen dynamics in an arid grassland. Ecol Appl 11:1301–1310. https://doi.org/10.1890/1051-0761(2001)011[1301:EPIAND]2.0.CO;2
Feng YL, Fu GL, Zheng YL (2008) Specific leaf area relates to the differences in leaf construction cost, photosynthesis, nitrogen allocation, and use efficiencies between invasive and noninvasive alien congeners. Planta 228:383–390. https://doi.org/10.1007/s00425-008-0732-2
Fisher MJ, Kerridge PC (1996) The Agronomy and Physiology of Brachiaria Species. In: Miles JW, Maass BL, Do Valle CB, Kumble V (eds) Brachiaria : biology, agronomy, and improvement. Centro Internacional de Agricultura Tropical, Cali, Colombia, pp 43–52
Flory SL, Clay K (2010a) Non-native grass invasion alters native plant composition in experimental communities. Biol Invasions 12:1285–1294. https://doi.org/10.1007/s10530-009-9546-9
Flory SL, Clay K (2010b) Non-native grass invasion suppresses forest succession. Oecologia 164:1029–1038. https://doi.org/10.1007/s00442-010-1697-y
Foxcroft LC, Richardson DM, Rejmánek M, Pyšek P (2010) Alien plant invasions in tropical and sub-tropical savannas: patterns, processes and prospects. Biol Invasions 12:3913–3933. https://doi.org/10.1007/s10530-010-9823-7
García-Díaz P, Cassey P, Norbury G et al (2021) Management policies for invasive alien species: addressing the impacts rather than the species. Bioscience 71:174–185. https://doi.org/10.1093/biosci/biaa139
García-Palacios P, Shaw EA, Wall DH, Hättenschwiler S (2016) Temporal dynamics of biotic and abiotic drivers of litter decomposition. Ecol Lett 19:554–563. https://doi.org/10.1111/ele.12590
Garcia DB, Xavier RO, Camargo PB et al (2022) Can an invasive African grass affect carbon and nitrogen stocks in open habitats of the Brazilian Cerrado? Flora 286:151968. https://doi.org/10.1016/J.FLORA.2021.151968
Gorgone-Barbosa E, Pivello VR, Bautista S et al (2015) How can an invasive grass affect fire behavior in a tropical savanna? A community and individual plant level approach. Biol Invasions 17:423–431. https://doi.org/10.1007/s10530-014-0740-z
Group TBF (2015) Growing knowledge: An overview of Seed Plant diversity in Brazil. Rodriguesia 66:1085–1113. https://doi.org/10.1590/2175-7860201566411
Guimarães Silva R, Zenni RD, Rosse VP et al (2020) Landscape-level determinants of the spread and impact of invasive grasses in protected areas. Biol Invasions 22:3083–3099. https://doi.org/10.1007/s10530-020-02307-4
Hoffmann WA, Haridasan M (2008) The invasive grass, Melinis minutiflora, inhibits tree regeneration in a Neotropical savanna. Austral Ecol 33:29–36. https://doi.org/10.1111/j.1442-9993.2007.01787.x
Holly DC, Ervin GN, Jackson CR et al (2009) Effect of an invasive grass on ambient rates of decomposition and microbial community structure: a search for causality. Biol Invasions 11:1855–1868. https://doi.org/10.1007/s10530-008-9364-5
Hui C, Richardson DM (2017) Invasion dynamics. Oxford University Press, Oxford
Huntley BJ, Walker BH (1982) Ecology of tropical Savannas. Springer, New York, USA
IBAMA IB do MA e dos RNR, FUNATURA. (1998) Plano de Manejo do Parque Nacional de Brasília.
IBGE (2004) Biomas Brasileiros. Mapa Temático. Instituto Brasileiro de Geografia e Estatística
Karberg NJ, Scott NA, Giardina CP (2008) Methods for Estimating Litter Decomposition. F Meas For Carbon Monit 103–111. https://doi.org/10.1007/978-1-4020-8506-2_8
Keith H, Wong SC (2006) Measurement of soil CO2efflux using soda lime absorption: both quantitative and reliable. Soil Biol Biochem 38:1121–1131. https://doi.org/10.1016/j.soilbio.2005.09.012
Lambers H, Oliveira RS (2019) Plant Physiological Ecology, 3rd Edit. Srpinger
Levine JM, Vilà M, D’Antonio CM et al (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc B Biol Sci 270:775–781. https://doi.org/10.1098/rspb.2003.2327
Lindsay EA, Cunningham SA (2012) Effects of exotic grass invasion on spatial heterogeneity in the ground-layer of grassy woodlands. Biol Invasions 14:203–213. https://doi.org/10.1007/s10530-011-9997-7
Litton CM, Sandquist DR, Cordell S (2006) Effects of non-native grass invasion on aboveground carbon pools and tree population structure in a tropical dry forest of Hawaii. For Ecol Manag 231:105–113. https://doi.org/10.1016/j.foreco.2006.05.008
Loiola PP, de Bello F, Chytrý M et al (2018) Invaders among locals: alien species decrease phylogenetic and functional diversity while increasing dissimilarity among native community members. J Ecol 106:2230–2241
Macena F, Assad E, Steinke ET, Gustavo Müller A (2008) Clima do Bioma Cerrado. In: Albuquerque ACS, Silva AG da (eds) Agricultura tropical: Quatro décadas de inovações tecnológicas, institucionais e políticas. Embrapa Informação Tecnológica, Brasília, pp 93–148
Milton SJ (2004) Grasses as invasive alien plants in South Africa. S Afr J Sci 100:69–75
Murphy BP, Andersen AN, Parr CL (2016) The underestimated biodiversity of tropical grassy biomes. Philos Trans R Soc B Biol Sci 371:1. https://doi.org/10.1098/rstb.2015.0319
Noss R (1990) Indicators for monitoring biodiversity: a hierarchical approach. Conserv Biol 4:355–364
Nuñez MA, Barlow J, Cadotte M et al (2019) Assessing the uneven global distribution of readership, submissions and publications in applied ecology: obvious problems without obvious solutions. J Appl Ecol 56:4–9. https://doi.org/10.1111/1365-2664.13319
Nuñez MA, Chiuffo MC, Pauchard A, Zenni RD (2021) Making ecology really global. Trends Ecol Evol 36:766–769. https://doi.org/10.1016/j.tree.2021.06.004
Parker I, Simberloff D, Lonsdale W (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19. https://doi.org/10.1023/A:1010034312781
Parr CL, Lehmann CER, Bond WJ et al (2014) Tropical grassy biomes: misunderstood, neglected, and under threat. Trends Ecol Evol 29:205–213. https://doi.org/10.1016/j.tree.2014.02.004
Pearse IS, Sofaer HR, Zaya DN, Spyreas G (2019) Non-native plants have greater impacts because of differing per-capita effects and nonlinear abundance-impact curves. Ecol Lett. https://doi.org/10.1111/ele.13284
Pérez-Harguindeguy N, Díaz S, Garnier E et al (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234. https://doi.org/10.1071/BT12225
Pilon NAL, Durigan G, Rickenback J, et al (2021) Shade alters savanna grass layer structure and function along a gradient of canopy cover. J Veg Sci 32:e12959. https://doi.org/10.1111/jvs.12959
Pivello VR, Coutinho LM (1996) A qualitative successional model to assist in the management of Brazilian cerrados. For Ecol Manag 87:127–138. https://doi.org/10.1016/S0378-1127(96)03829-7
Pivello VR, Shida CN, Meirelles ST (1999) Alien grasses in Brazilian savannas: A threat to the biodiversity. Biodivers Conserv 8:1281–1294. https://doi.org/10.1023/A:1008933305857
R Core Team (2020) R: a language and environment for statistical computing
Reed HE, Seastedt TR, Blair JM (2005) Ecological consequences of C 4 grass invasion of a C 4 Grassland: a dilemma for management. Ecol Appl 15:1560–1569. https://doi.org/10.1890/04-0407
Rosenfeld JS (2002) Functional redundancy in ecology and conservation. Oikos 98:156–162
Rossiter-Rachor NA, Setterfield SA, Douglas MM et al (2009) Invasive Andropogon gayanus (gamba grass) is an ecosystem transformer of nitrogen relations in Australian savanna. Ecol Appl 19:1546–1560. https://doi.org/10.1890/08-0265.1
Rossiter NA, Setterfield SA, Douglas MM, Hutley LB (2003) Testing the grass-fire cycle: alien grass invasion in the tropical savannas of northern Australia. Divers Distrib 9:169–176. https://doi.org/10.1046/j.1472-4642.2003.00020.x
Setterfield SA, Rossiter-Rachor NA, Douglas MM, et al (2013) Adding fuel to the fire: the impacts of non-native grass invasion on fire management at a regional scale. PLoS One 8:e59144. https://doi.org/10.1371/journal.pone.0059144
Silva JSO, Haridasan M (2007) Acúmulo de biomassa aérea e concentração de nutrientes em Melinis minutiflora P. Beauv. e gramíneas nativas do cerrado. Rev Bras Botânica 30:337–344. https://doi.org/10.1590/S0100-84042007000200016
Silveira Sartori M (2012) Diversidade de comunidades bacterianas de solo de Cerrado em resposta a diferentes alterações dos ecossistemas. 140
Smith VC, Bradford MA (2003) Litter quality impacts on grassland litter decomposition are differently dependent on soil fauna across time. Appl Soil Ecol 24:197–203. https://doi.org/10.1016/S0929-1393(03)00094-5
Sofaer HR, Jarnevich CS, Pearse IS (2018) The relationship between invader abundance and impact. Ecosphere 9:1. https://doi.org/10.1002/ecs2.2415
Souza CM, Shimbo JZ, Rosa MR et al (2020) Reconstructing three decades of land use and land cover changes in brazilian biomes with landsat archive and earth engine. Remote Sens 12:1
Strassburg BBN, Brooks T, Feltran-Barbieri R et al (2017) Moment of truth for the Cerrado hotspot. Nat Ecol Evol 1:1–3. https://doi.org/10.1038/s41559-017-0099
Strayer DL (2020) Non-native species have multiple abundance-impact curves. Ecol Evol. https://doi.org/10.1002/ece3.6364
Vila M, Basnou C, Pysek P et al (2010) How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front Ecol Environ 8:135–144. https://doi.org/10.1890/080083
Vila M, Espinar JL, Hejda M et al (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708. https://doi.org/10.1111/j.1461-0248.2011.01628.x
Wickham H (2009) ggplot2: Elegant graphics for data analysis. Springer, New York
Wikum DA, Shanholtzer GF (1978) Application of the Braun-Blanquet cover-abundance scale for vegetation analysis in land development studies. Environ Manage 2:323–329. https://doi.org/10.1007/BF01866672
Wilke CO (2019) cowplot: Streamlined Plot Theme and Plot Annotations for “ggplot2”
Wilsey BJ, Daneshgar PP, Hofmockel K, Polley HW (2014) Invaded grassland communities have altered stability-maintenance mechanisms but equal stability compared to native communities. Ecol Lett 17:92–100. https://doi.org/10.1111/ele.12213
Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc Ser B 73:3–36. https://doi.org/10.7538/yzk.2014.48.11.1969
Yokomizo H, Possingham HP, Thomas MB, Buckley YM (2009) Managing the impact of invasive species: the value of knowing the density-impact curve. Ecol Appl 19:376–386
Zanchetta D, Delgado J, Silva C, et al (2006) Plano de Manejo Integrado: Estações Ecológica e Experimental de Itirapina/SP, 1a Revisão. Instituto Florestal de São Paulo, São Paulo, Brazil
Zanchi FB, Waterloo MJ, Aguiar LJG et al (2009) Estimativa do Índice de Área Foliar (IAF) e Biomassa em pastagem no estado de Rondônia, Brasil. Acta Amaz 39:335–347. https://doi.org/10.1590/s0044-59672009000200012
Zenni RD, Cunha WL, Musso C et al (2020) Synergistic impacts of co-occurring invasive grasses cause persistent effects in the soil-plant system after selective removal. Funct Ecol 34:1102–1112. https://doi.org/10.1111/1365-2435.13524
Acknowledgements
Authors thank Amanda Viana, Cassy Anne Santos, Daniel Borini, Giovana Chiari, Heloiza Zirondi, Juliana Teixeira, Marco Chiminazzo, Mariana Dairel, Soizig Le Stradic, Tamires Zepon, Vagner Zanzarini and Yara Ballarini for their help during field work. We also thank people in the CONTAIN project for great discussions about invasive species in general. We are grateful to Giselda Durigan, Alexandre Sampaio, Carlos Romero Martins, Lara Souza, Michele Dechoum, Vania Pivello and the anonymous reviewers for their valuable comments on previous versions of this manuscript. Permissions to conduct the experiment were given by authorizations SISBIO nº63040 and COTEC 260108 – 005.306/2018.
Funding
This study was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (2018/09054-0, G.D., scholarship; 2015/06743–0, 2018/14995-8, A.F. research project) and the Neotropical Grasslands Conservancy. G.D. and A.F. are part of the Project CONTAIN—‘Optimising the long-term management of invasive species affecting biodiversity and the rural economy using adaptive management’, partially funded by Natural Environment Research Council—NERC, under the Latin American Biodiversity Programme as part of the Newton Fund (NE/S011641/1). This study was financed in part by the Coordenaçãoo de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)—Finance Code 001. Additionally, A.F. receives grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, # 312689/2021–7).
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Both authors contributed to the study conception and design. Data collection, sampling, processing and analysis were performed by Gabriella Damasceno. The first draft was written by Gabriella Damasceno and Alessandra Fidelis commented on all previous versions of the manuscript. Both authors read and approved the final manuscript.
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Damasceno, G., Fidelis, A. Per-capita impacts of an invasive grass vary across levels of ecological organization in a tropical savanna. Biol Invasions 25, 1811–1826 (2023). https://doi.org/10.1007/s10530-023-03011-9
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DOI: https://doi.org/10.1007/s10530-023-03011-9