Abstract
Worldwide, invasive alien plant species (IAS) threaten the biodiversity and the functioning of ecosystems. Most invasion research so far has focused on the properties underlying species invasiveness and community invasibility, yet IAS impact and the underlying causal pathways remain largely unknown. Here we dealt with this knowledge gap by extending the traditional functional trait framework to spectral data, by using traits estimated from reflectance measurements obtained through proximal field spectroscopy, as a surrogate for conventionally measured traits. We focused on two functionally distinct species that are invasive in Belgium: the annual forb Impatiens glandulifera Royle, and the rhizomatous perennial forb Solidago gigantea Ait. By means of trait-based linear mixed models and structural equation models we studied their impact on six ecosystem functions involved in the cycling of carbon and nutrients, and the mechanisms mediating these changes. Analyses based on either conventionally or optically measured traits revealed similar results: the IAS altered aboveground biomass (decrease and increase under I. glandulifera and S. gigantea respectively), litter stabilization (decrease under both IAS) and soil available phosphorus (increase under both IAS) through mass ratio effects, rather than through decreasing the functional diversity of the community. Whereas S. gigantea did so by shifting the community towards more conservative traits, I. glandulifera achieved this by making the community taller and richer in leaf nutrients. The use of remote sensing through optically measured traits, is not only useful to advance our understanding of the mechanisms and consequences of plant invasion, but may also be valuable to the broader field linking plant community composition to ecosystem functioning. Its potential for studying larger spatial scales over time may contribute to even more comprehensive insights.
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References
Abelleira Martínez OJ, Fremier AK, Günter S et al (2016) Scaling up functional traits for ecosystem services with remote sensing: concepts and methods. Ecol Evol 6:4359–4371. https://doi.org/10.1002/ece3.2201
Ali A, Yan E, Chang SX et al (2017) Community-weighted mean of leaf traits and divergence of wood traits predict aboveground biomass in secondary subtropical forests. Sci Total Environ 574:654–662. https://doi.org/10.1016/j.scitotenv.2016.09.022
Barton K (2018) MuMIn: Multi-Model Inference. R Packag. version 1.42.1
Bates DM, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.1177/009286150103500418
Beerling DJ, Perrins JM (1993) Impatiens glandulifera Royle (Impatiens Roylei Walp.). J Ecol 81:367–382. https://doi.org/10.2307/2261507
Branquart E (2019) Alert, black and watch lists of invasive species in Belgium. Harmonia version 1.2. In: Belgian Forum on Invasive species
Bruelheide H, Dengler J, Purschke O et al (2018) Global trait–environment relationships of plant communities. Nat Ecol Evol 2:1906–1917. https://doi.org/10.1038/s41559-018-0699-8
Cadotte MW (2017) Functional traits explain ecosystem function through opposing mechanisms. Ecol Lett 20:989–996. https://doi.org/10.1111/ele.12796
Castro-Díez P, Pauchard A, Traveset A et al (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
Chapuis-Lardy L, Vanderhoeven S, Dassonville N et al (2006) Effect of the exotic invasive plant Solidago gigantea on soil phosphorus status. Biol Fertil Soils 42:481–489. https://doi.org/10.1007/s00374-005-0039-4
Chittka L, Schürkens S (2001) Successful invasion of a floral market. Nature 411:653–653. https://doi.org/10.1038/35079676
DAISIE (2009) Handbook of alien species in Europe. Springer, Netherlands
Dassonville N, Vanderhoeven S, Vanparys V et al (2008) Impacts of alien invasive plants on soil nutrients are correlated with initial site conditions in NW Europe. Oecologia 157:131–140. https://doi.org/10.1007/s00442-008-1054-6
de Bello F, Lavorel S, Díaz S et al (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893. https://doi.org/10.1007/s10531-010-9850-9
de Vries FT, Manning P, Tallowin JRB et al (2012) Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities. Ecol Lett 15:1230–1239. https://doi.org/10.1111/j.1461-0248.2012.01844.x
Drenovsky RE, Grewell BJ, Dantonio CM et al (2012) A functional trait perspective on plant invasion. Ann Bot 110:141–153. https://doi.org/10.1093/aob/mcs100
Dukes JS (2002) Species composition and diversity affect grassland susceptibility and response to invasion. Ecol Appl 12:602–617
Ewald M, Skowronek S, Aerts R et al (2018) Analyzing remotely sensed structural and chemical canopy traits of a forest invaded by Prunus serotina over multiple spatial scales. Biol Invasions 20:2257–2271. https://doi.org/10.1007/s10530-018-1700-9
Feilhauer H, Asner GP, Martin RE, Schmidtlein S (2010) Brightness-normalized partial least squares regression for hyperspectral data. J Quant Spectrosc Radiat Transf 111:1947–1957. https://doi.org/10.1016/j.jqsrt.2010.03.007
Finerty GE, de Bello F, Bílá K et al (2016) Exotic or not, leaf trait dissimilarity modulates the effect of dominant species on mixed litter decomposition. J Ecol 104:1400–1409. https://doi.org/10.1111/1365-2745.12602
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks CA
Fynn RW, Wragg PD, Morris CD et al (2009) Vegetative traits predict grass species’ invasiveness and the invasibility of restored grassland. African J Range Forage Sci 26:59–68. https://doi.org/10.2989/AJRFS.2009.26.2.2.845
Garnier E, Cortez J, Billès G et al (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637. https://doi.org/10.1890/03-0799
Gower JC (1975) Generalized procrustes analysis. Psychometrika 40:33–51. https://doi.org/10.1007/BF02291478
Grace JB, Anderson TM, Seabloom EW et al (2016) Integrative modelling reveals mechanisms linking productivity and plant species richness. Nature 529:390–393. https://doi.org/10.1038/nature16524
Grime (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910. https://doi.org/10.1046/j.1365-2745.1998.00306.x
Grime JP (2001) Plant strategies, vegetation processes, and ecosystem properties, 2nd edn. Wiley, Chichester
Gross N, Suding KN, Lavorel S, Roumet C (2007) Complementarity as a mechanism of coexistence between functional groups of grasses. J Ecol 95:1296–1305. https://doi.org/10.1111/j.1365-2745.2007.01303.x
Große-Stoltenberg A, Hellmann C, Thiele J et al (2018) Invasive acacias differ from native dune species in the hyperspectral/biochemical trait space. J Veg Sci 29:325–335. https://doi.org/10.1111/jvs.12608
Güsewell S, Zuberbühler N, Clerc C (2005) Distribution and functional traits of Solidago gigantea in a Swiss lakeshore wetland. Bot Helv 115:63–75. https://doi.org/10.1007/s00035-005-0721-z
Güsewell S, Jakobs G, Weber E (2006) Native and introduced populations of Solidago gigantea differ in shoot production but not in leaf traits or litter decomposition. Funct Ecol. https://doi.org/10.1111/j.1365-2435.2006.01141.x
Harrison XA, Donaldson L, Correa-Cano ME et al (2018) A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 6:e4794. https://doi.org/10.7717/peerj.4794
Hejda M, de Bello F (2013) Impact of plant invasions on functional diversity in the vegetation of Central Europe. J Veg Sci 24:890–897. https://doi.org/10.1111/jvs.12026
Hejda M, Pyšek P (2006) What is the impact of Impatiens glandulifera on species diversity of invaded riparian vegetation? Biol Conserv 132:143–152. https://doi.org/10.1016/j.biocon.2006.03.025
Hejda M, Pyšek P, Jarošík V (2009) Impact of invasive plants on the species richness, diversity and composition of invaded communities. J Ecol 97:393–403. https://doi.org/10.1111/j.1365-2745.2009.01480.x
Helsen K, Kapás RE, Rakvaag G et al (2018a) Impacts of an invasive plant on primary production: testing a functional trait-based framework with a greenhouse experiment. J Veg Sci 29:157–166. https://doi.org/10.1111/jvs.12619
Helsen K, Smith SW, Brunet J et al (2018b) Impact of an invasive alien plant on litter decomposition along a latitudinal gradient. Ecosphere. https://doi.org/10.1002/ecs2.2097
Helsen K, Van Cleemput E, Bassi L et al (2020a) Inter- and intraspecific trait variation shape multidimensional trait overlap between two plant invaders and the invaded communities. Oikos 129:677–688
Helsen K, Van Cleemput E, Bassi L et al (2020b) Optical traits perform equally well as directly-measured functional traits in explaining the impact of an invasive plant on litter decomposition. J Ecol 1365–2745:13389. https://doi.org/10.1111/1365-2745.13389
Herr C, Chapuis-Lardy L, Dassonville N et al (2007) Seasonal effect of the exotic invasive plant Solidago gigantea on soil pH and P fractions. J Plant Nutr Soil Sci 170:729–738. https://doi.org/10.1002/jpln.200625190
Homolová L, Malenovský Z, Clevers JGPW et al (2013) Review of optical-based remote sensing for plant trait mapping. Ecol Complex 15:1–16. https://doi.org/10.1016/j.ecocom.2013.06.003
Hulme PE, Bernard-Verdier M (2018) Comparing traits of native and alien plants: can we do better? Funct Ecol 32:117–125. https://doi.org/10.1111/1365-2435.12982
Jetz W, Cavender-Bares J, Pavlick R et al (2016) Monitoring plant functional diversity from space. Nat Plants 2:28–31. https://doi.org/10.1038/NPLANTS.2016.24
Jewell MD, Shipley B, Low-décarie E et al (2017) Partitioning the effect of composition and diversity of tree communities on leaf litter decomposition and soil respiration. Oikos 126:959–971. https://doi.org/10.1111/oik.03868
Keuskamp JA, Dingemans BJJ, Lehtinen T et al (2013) Tea bag index: a novel approach to collect uniform decomposition data across ecosystems. Methods Ecol Evol 4:1070–1075. https://doi.org/10.1111/2041-210X.12097
Laliberte E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits A distance-based framework for measuring from multiple traits functional diversity. Ecology 91:299–305. https://doi.org/10.1890/08-2244.1
Laliberté E, Legendre P, Shipley B (2014) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R Packag. version 1.0-12
Lausch A, Leitão PJ (2018) Monitoring vegetation diversity and health through spectral traits and trait variations based on hyperspectral remote sensing. In: Thenkabail PS, Lyon GJ, Huete A (eds) Hyperspectral remote sensing of vegetation. CRC Press, New York, pp 95–126
Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16:545–556. https://doi.org/10.1046/j.1365-2435.2002.00664.x
Lavorel S, Grigulis K, McIntyre S et al (2008) Assessing functional diversity in the field-methodology matters! Funct Ecol 22:134–147. https://doi.org/10.1111/j.1365-2435.2007.01339.x
Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512
Londo G (1976) The decimal scale for releves of permanent quadrats. Vegetatio 33:61–64. https://doi.org/10.1007/BF00055300
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76. https://doi.org/10.1038/35083573
Macel M, de Vos RCH, Jansen JJ et al (2014) Novel chemistry of invasive plants: exotic species have more unique metabolomic profiles than native congeners. Ecol Evol 4:2777–2786. https://doi.org/10.1002/ece3.1132
Mevik B-H, Wehrens R, Liland KH (2018) pls: Partial Least Squares and Principal Component Regression. R Packag. version 2.7-0
Mládková P, Mládek J, Hejduk S et al (2018) Calcium plus magnesium indicates digestibility: the significance of the second major axis of plant chemical variation for ecological processes. Ecol Lett 21:885–895. https://doi.org/10.1111/ele.12956
Mokany K, Ash J, Roxburgh S (2008) Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. J Ecol 96:884–893. https://doi.org/10.1111/j.1365-2745.2008.01395.x
Oksanen J, Blanchet FG, Friendly M et al (2019) Vegan: community ecology package. R Packag version. https://doi.org/10.1093/molbev/msv334
Olden JD, Poff NLR, Douglas MR et al (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24. https://doi.org/10.1016/j.tree.2003.09.010
Oliver TH, Heard MS, Isaac NJB et al (2015) Biodiversity and resilience of ecosystem functions. Trends Ecol Evol 30:673–684. https://doi.org/10.1016/j.tree.2015.08.009
Ollinger SV (2011) Sources of variability in canopy reflectance and the convergent properties of plants. New Phytol 189:375–394. https://doi.org/10.1111/j.1469-8137.2010.03536.x
Olsen SR (1954) Estimation of Available phosphorus in soils by extraction with sodium bicarbonate. Circ United States Dept Agric 939:1–19
Orwin KH, Buckland SM, Johnson D et al (2010) Linkages of plant traits to soil properties and the functioning of temperate grassland. J Ecol 98:1074–1083. https://doi.org/10.1111/j.1365-2745.2010.01679.x
Pakeman RJ, Quested HM (2007) Sampling plant functional traits: what proportion of the species need to be measured? Appl Veg Sci 10:91–96. https://doi.org/10.1111/j.1654-109X.2007.tb00507.x
Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24:497–504. https://doi.org/10.1016/j.tree.2009.03.016
Pérez-Harguindeguy N, Diaz S, Garnier E et al (2013) New Handbook for standardized measurment of plant functional traits worldwide. Aust J Bot 61:167–234. https://doi.org/10.1071/BT12225
Pinheiro J, Bates D, DebRoy S, et al (2018) nlme: Linear and Nonlinear Mixed Effects Models. R Packag. version 3.1-137
Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Biological invasions. Ecological studies (Analysis and Synthtesis). Springer, Berlin, pp 97–125
Pyšek P, Richardson DM (2010) Invasive species, environmental change and management, and health. Annu Rev Environ Resour 35:25–55. https://doi.org/10.1146/annurev-environ-033009-095548
Pyšek P, Jarošík V, Hulme PE et al (2012) A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Glob Chang Biol 18:1725–1737. https://doi.org/10.1111/j.1365-2486.2011.02636.x
RStudio (2016) RStudio: Integrated Development for R. RStudio, Inc
Ruckli R, Rusterholz HP, Baur B (2013) Invasion of Impatiens glandulifera affects terrestrial gastropods by altering microclimate. Acta Oecol 47:16–23. https://doi.org/10.1016/j.actao.2012.10.011
Ruckli R, Hesse K, Glauser G et al (2014a) Inhibitory potential of naphthoquinones leached from leaves and exuded from roots of the invasive plant Impatiens glandulifera. J. Chem. Ecol 40:371–378. https://doi.org/10.1007/s10886-014-0421-5
Ruckli R, Rusterholz H, Baur B (2014b) Invasion of an annual exotic plant into deciduous forests suppresses arbuscular mycorrhiza symbiosis and reduces performance of sycamore maple saplings. For Ecol Manage 318:285–293. https://doi.org/10.1016/j.foreco.2014.01.015
Santos MJ, Hestir EL, Khanna S, Ustin SL (2012) Image spectroscopy and stable isotopes elucidate functional dissimilarity between native and nonnative plant species in the aquatic environment. New Phytol 193:683–695. https://doi.org/10.1111/j.1469-8137.2011.03955.x
Scharfy D, Eggenschwiler H, Olde Venterink H et al (2009) The invasive alien plant species Solidago gigantea alters ecosystem properties across habitats with differing fertility. J Veg Sci 20:1072–1085. https://doi.org/10.1111/j.1654-1103.2009.01105.x
Seebens H, Blackburn TM, Dyer EE et al (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8:1–9. https://doi.org/10.1038/ncomms14435
Shipley B (2000) A new inferential test for path models based on directed acyclic graphs. Struct Equ Model A Multidiscip J 7:206–218. https://doi.org/10.1207/S15328007SEM0702_4
Skowronek S, Ewald M, Isermann M et al (2017) Mapping an invasive bryophyte species using hyperspectral remote sensing data. Biol Invasions 19:239–254. https://doi.org/10.1007/s10530-016-1276-1
Somers B, Asner GP (2013) Invasive species mapping in hawaiian rainforests using multi-temporal hyperion spaceborne imaging spectroscopy. IEEE J Sel Top Appl Earth Obs Remote Sens 6:351–359. https://doi.org/10.1109/JSTARS.2012.2203796
Stuckens J, Somers B, Verstraeten WW et al (2009) Evaluation and normalization of cloud obscuration related BRDF effects in field spectroscopy. Remote Sens 1:496–518. https://doi.org/10.3390/rs1030496
Tanner RA, Varia S, Eschen R et al (2013) Impacts of an invasive non-native annual weed, Impatiens glandulifera, on above- and below-ground invertebrate communities in the United Kingdom. PLoS ONE 8(6):e67271. https://doi.org/10.1371/journal.pone.0067271
Van Buuren S, Groothuis-Oudshoorn K (2011) mice: multivariate imputation by chained equations in R. J Stat Softw 45:1–67
Van Cleemput E, Vanierschot L, Fernández-Castilla B et al (2018) The functional characterization of grass- and shrubland ecosystems using hyperspectral remote sensing: trends, accuracy and moderating variables. Remote Sens Environ 209:747–763. https://doi.org/10.1016/j.rse.2018.02.030
Van Cleemput E, Roberts DA, Honnay O, Somers B (2019) A novel procedure for measuring functional traits of herbaceous species through field spectroscopy. Methods Ecol Evol 10:1332–1338. https://doi.org/10.1111/2041-210X.13237
Van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245. https://doi.org/10.1111/j.1461-0248.2009.01418.x
Vanderhoeven S, Dassonville N, Chapuis-Lardy L et al (2006) Impact of the invasive alien plant Solidago gigantea on primary productivity, plant nutrient content and soil mineral nutrient concentrations. Plant Soil 286:259–268. https://doi.org/10.1007/s11104-006-9042-2
Vilà 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
Wardle DA, Bardgett RD, Callaway RM, Van der Putten WH (2011) Terrestrial ecosystem responses to species gains and losses. Science 332:1273–1277. https://doi.org/10.1126/science.1197479
Weber E, Jakobs G (2005) Biological flora of central Europe: Solidago gigantea Aiton. Flora 200:109–118. https://doi.org/10.1016/j.flora.2004.09.001
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821. https://doi.org/10.1038/nature02403
Zhu J, Jiang L, Zhang Y (2016) Relationships between functional diversity and aboveground biomass production in the Northern Tibetan alpine grasslands. Sci Rep 6:34105. https://doi.org/10.1038/srep34105
Acknowledgements
We would like to thank everyone who participated in the data collection, in particular Remi Chevalier, Bert Symons and Pieter Meert. This study was funded by the Belgian Science Policy Office in the framework of the STEREOIII program (projects INPLANT (SR/01/321) and INPLANT2.0 (SR/01/391)), and internal KU Leuven funding (Special Research Fund, C1 project).
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The paired dataset on species-level reflectance and conventionally measured traits is stored in the EcoSIS library (https://doi.org/10.21232/ss03-g783). The conventionally measured trait values are also stored in the TRY database (dataset ID 617). Data on the tea bag metrics are submitted to the global TBI database (http://www.teatime4science.org/).
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Van Cleemput, E., Van Meerbeek, K., Helsen, K. et al. Remotely sensed plant traits can provide insights into ecosystem impacts of plant invasions: a case study covering two functionally different invaders. Biol Invasions 22, 3533–3550 (2020). https://doi.org/10.1007/s10530-020-02338-x
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DOI: https://doi.org/10.1007/s10530-020-02338-x