Abstract
Bioinvasions pose undeniable threats and trigger changes in salt marsh ecosystem functioning. In Mediterranean and Atlantic marshes, the invasion by S. patens contributed to added competitive pressure to native middle-upper marsh species such as H. portulacoides. The introduction of a new and aggressive non-indigenous species (NIS) is a game-changer for the marsh biogeochemical functioning. In the present study we explored effects of this bioinvasion on an array of different extracellular enzymatic activities (EEA) of salt marsh sediments colonized by NIS and native plant species and its impacts on the biogeochemical functioning of a large estuarine ecosystem. In H. portulacoides there was an evident control of the extracellular enzymatic activities (EEA) by the sediment physic-chemical traits, but these relationships were weaker and fewer in number when compared to the EEA and the sediment abiotic traits in the sediments colonized by S. patens. This indicates a prevalence of a plant effect over abiotic traits in controlling EEA. Disruption in biogeochemical functioning was evident in the sediments colonized by S. patens, with clear enzymatic activity peaks during spring and summer and with significantly higher values of several EEA during autumn and winter. These led to an acceleration of necromass decomposition processes and thus to reduced marsh storage and remediation capacity. Spartina patens also showed increased phosphatase, urease, and protease activity contributing to increased release of the inorganic phosphorous and nitrogen (ammonia) into the system. Higher activity of carbon-based substrates decomposition allied to an increase in dehydrogenase activity (proxy to microbial abundance and respiration), will lead to an inevitable decrease in the carbon sink capacity of the sediments and reduction of the blue carbon storage ecosystem service. The sulfatase activity in the S. patens rhizosediments also showed a significant decrease during autumn, leading to reduced production of sulfate, sulfides and increased metal bioavailability. All these changes amount to a loss of the sink capacity of the system, in terms of eutrophication reduction through organic nitrogen and phosphorous retention, carbon sink due to the acceleration of the decomposition processes and decreased metal remediation capacity. Thus, the present work highlights the need to control this invasive species not only to prevent potential reductions in floristic diversity but also to prevent the loss of key biogeochemical services, that can impact the entire estuarine system.
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References
Adams JB (2020) Salt marsh at the tip of Africa: patterns, processes and changes in response to climate change. Estuar Coast Shelf Sci 237:106650. https://doi.org/10.1016/j.ecss.2020.106650
Alef K, Nannipieri P (1995) 7-Enzyme activities. Methods in applied soil microbiology and biochemistry. Academic Press, London, pp 311–373
Alonso-Sáez L, Vázquez-Domínguez E, Cardelús C et al (2008) Factors controlling the year-round variability in carbon flux through bacteria in a coastal marine system. Ecosystems 11:397–409. https://doi.org/10.1007/s10021-008-9129-0
Aminot A, Kirkwood DS, Kérouel R (1997) Determination of ammonia in seawater by the indophenol-blue method: evaluation of the ICES NUTS I/C 5 questionnaire. Mar Chem 56:59–75. https://doi.org/10.1016/S0304-4203(96)00080-1
Anjum NA, Ahmad I, Válega M et al (2014) Salt marsh halophyte services to metal-metalloid remediation: assessment of the processes and underlying mechanisms. Crit Rev Environ Sci Technol 44:2038–2106. https://doi.org/10.1080/10643389.2013.828271
Aroca A, Gotor C, Bassham DC, Romero LC (2020) Hydrogen sulfide: from a toxic molecule to a key molecule of cell life. Antioxidants 9:621. https://doi.org/10.3390/antiox9070621
Asanopoulos CH, Baldock JA, Macdonald LM et al (2021) Quantifying blue carbon and nitrogen stocks in surface soils of temperate coastal wetlands. Soil Res. https://doi.org/10.1071/SR20040
Aşkın T, Kızılkaya R (2006) Assessing spatial variability of soil enzyme activities in pasture topsoils using geostatistics. Eur J Soil Biol 42:230–237. https://doi.org/10.1016/j.ejsobi.2006.02.002
Baumel A, Rousseau-Gueutin M, Sapienza-Bianchi C et al (2016) Spartina versicolor Fabre: Another case of Spartina trans-Atlantic introduction? Biol Invasions 18:2123–2135. https://doi.org/10.1007/s10530-016-1128-z
Benner R, Newell SY, Maccubbin AE, Hodson RE (1984) Relative contributions of bacteria and fungi to rates of degradation of lignocellulosic detritus in salt-marsh sediments. Appl Environ Microbiol 48:36–40. https://doi.org/10.1128/aem.48.1.36-40.1984
Bertness MD, Shumway SW (1993) Competition and facilitation in marsh plants. Am Nat 142:718–724. https://doi.org/10.1086/285567
Borges FO, Santos CP, Paula JR et al (2021) Invasion and extirpation potential of native and invasive spartina species under climate change. Front Mar Sci 8:1157. https://doi.org/10.3389/fmars.2021.696333
Bortolus A, Adam P, Adams JBBJBJBJB et al (2019) Supporting spartina: interdisciplinary perspective shows spartina as a distinct solid genus. Ecology 100:1–6. https://doi.org/10.1002/ecy.2863
Brewer JS, Rand T, Levine JM, Bertness MD (1998) Biomass allocation, clonal dispersal, and competitive success in three salt marsh plants. Oikos 82:347–353. https://doi.org/10.2307/3546975
Bulseco AN, Vineis JH, Murphy AE et al (2020) Metagenomics coupled with biogeochemical rates measurements provide evidence that nitrate addition stimulates respiration in salt marsh sediments. Limnol Oceanogr 65:S321–S339. https://doi.org/10.1002/lno.11326
Caçador I, Caetano M, Duarte B, Vale C (2009) Stock and losses of trace metals from salt marsh plants. Mar Environ Res 67:75–82. https://doi.org/10.1016/j.marenvres.2008.11.004
Caçador I, Neto JM, Duarte B et al (2013) Development of an angiosperm quality assessment index (AQuA-Index) for ecological quality evaluation of portuguese water bodies—a multi-metric approach. Ecol Ind 25:141–148. https://doi.org/10.1016/j.ecolind.2012.09.021
Caravaca F, Alguacil MM, Torres P, Roldán A (2005) Plant type mediates rhizospheric microbial activities and soil aggregation in a semiarid Mediterranean salt marsh. Geoderma 124:375–382. https://doi.org/10.1016/j.geoderma.2004.05.010
Carlton JT (1996) Marine bioinvasions: the alteration of marine ecosystems by nonindigenous species. Oceanography 9:36–43
Castillo JM, Leira-Doce P, Figueroa E (2017) Biomass and clonal architecture of the cordgrass spartina patens (poaceae) as an invasive species in two contrasted coastal habitats on the Atlantic coast of the Iberian peninsula. Plant Ecology and Evolution 150:129–138. https://doi.org/10.5091/plecevo.2017.1290
Chakraborty SK (2019) Bioinvasion and environmental perturbation: synergistic impact on coastal-mangrove ecosystems of West Bengal India. In: Makowski C, Finkl CW (eds) Impacts of invasive species on coastal environments: coasts in crisis. Springer International Publishing, Cham, pp 171–245
Chaudhary DR, Kim J, Kang H (2018) Influences of different halophyte vegetation on soil microbial community at temperate salt marsh. Microb Ecol 75:729–738. https://doi.org/10.1007/s00248-017-1083-y
Cheng X, Luo Y, Chen J et al (2006) Short-term C4 plant Spartina alterniflora invasions change the soil carbon in C3 plant-dominated tidal wetlands on a growing estuarine Island. Soil Biol Biochem 38:3380–3386. https://doi.org/10.1016/j.soilbio.2006.05.016
Colmer TD, Flowers TJ (2008) Flooding tolerance in halophytes. New Phytol 179:964–974. https://doi.org/10.1111/j.1469-8137.2008.02483.x
Costa AL, Paixão SM, Caçador I, Carolino M (2007) CLPP and EEA profiles of microbial communities in salt marsh sediments. J Soils Sediments 7:418–425. https://doi.org/10.1065/jss2007.02.211
Couto N, Ferreira AR, Guedes P et al (2018) Remediation potential of caffeine, oxybenzone, and triclosan by the salt marsh plants Spartina maritima and Halimione portulacoides. Environ Sci Pollut Res 25:35928–35935. https://doi.org/10.1007/s11356-018-3042-7
Daehler CC, Strong DR (1996) Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in Pacific estuaries, USA. Biol Cons 78:51–58. https://doi.org/10.1016/0006-3207(96)00017-1
Dibble KL, Pooler PS, Meyerson LA (2013) Impacts of plant invasions can be reversed through restoration: a regional meta-analysis of faunal communities. Biol Invasions 15:1725–1737. https://doi.org/10.1007/s10530-012-0404-9
Domingues RB, Barbosa AB, Sommer U, Galvão HM (2011) Ammonium, nitrate and phytoplankton interactions in a freshwater tidal estuarine zone: potential effects of cultural eutrophication. Aquat Sci 73:331–343. https://doi.org/10.1007/s00027-011-0180-0
Duarte B, Almeida PRR, Caçador I (2009) Spartina maritima (cordgrass) rhizosediment extracellular enzymatic activity and its role in organic matter decomposition processes and metal speciation. Mar Ecol 30:65–73. https://doi.org/10.1111/j.1439-0485.2009.00326.x
Duarte B, Baeta A, Rousseau-Gueutin M et al (2015a) A tale of two spartinas: climatic, photobiological and isotopic insights on the fitness of non-indigenous versus native species. Estuar Coast Shelf Sci 167:178–190. https://doi.org/10.1016/j.ecss.2015.06.015
Duarte B, Caçador I (2021) Iberian halophytes as agroecological solutions for degraded lands and biosaline agriculture. Sustainability 13:1005. https://doi.org/10.3390/su13021005
Duarte B, Caetano M, Almeida PR et al (2010) Accumulation and biological cycling of heavy metal in four salt marsh species, from Tagus estuary (Portugal). Environ Pollut 158:1661–1668. https://doi.org/10.1016/j.envpol.2009.12.004
Duarte B, Carreiras J, Caçador I (2021) Climate change impacts on salt marsh blue carbon, nitrogen and phosphorous stocks and ecosystem services. Appl Sci 11:1969. https://doi.org/10.3390/app11041969
Duarte B, Freitas J, Caçador I (2011) The role of organic acids in assisted phytoremediation processes of salt marsh sediments. Hydrobiologia 674:169–177. https://doi.org/10.1007/s10750-011-0731-3
Duarte B, Freitas J, Caçador I (2012) Sediment microbial activities and physic-chemistry as progress indicators of salt marsh restoration processes. Ecol Ind 19:231–239. https://doi.org/10.1016/j.ecolind.2011.07.014
Duarte B, Freitas J, Couto T et al (2013a) New multi-metric Salt Marsh Sediment Microbial Index (SSMI) application to salt marsh sediments ecological status assessment. Ecol Ind 29:390–397. https://doi.org/10.1016/j.ecolind.2013.01.008
Duarte B, Freitas J, Valentim J et al (2014a) Abiotic control modelling of salt marsh sediments respiratory CO2 fluxes: application to increasing temperature scenarios. Ecol Ind 46:110–118. https://doi.org/10.1016/j.ecolind.2014.06.018
Duarte B, Marques JC, Caçador I (2016) Ecophysiological response of native and invasive Spartina species to extreme temperature events in Mediterranean marshes. Biol Invasions 18:2189–2205. https://doi.org/10.1007/s10530-015-0958-4
Duarte B, Mateos-Naranjo E, Goméz SR et al (2018) Cordgrass invasions in mediterranean marshes: past, present and future. In: Queiroz AI, Pooley S (eds) Histories of bioinvasions in the mediterranean. Springer International Publishing, Cham, pp 171–193
Duarte B, Reboreda R, Caçador I (2008) Seasonal variation of extracellular enzymatic activity (EEA) and its influence on metal speciation in a polluted salt marsh. Chemosphere 73:1056–1063. https://doi.org/10.1016/j.chemosphere.2008.07.072
Duarte B, Santos D, Marques JC, Caçador I (2015b) Ecophysiological constraints of two invasive plant species under a saline gradient: halophytes versus glycophytes. Estuar Coast Shelf Sci 167:154–165. https://doi.org/10.1016/j.ecss.2015.04.007
Duarte B, Santos D, Marques JC, Caçador I (2013b) Ecophysiological adaptations of two halophytes to salt stress: Photosynthesis, PS II photochemistry and anti-oxidant feedback – Implications for resilience in climate change. Plant Physiol Biochem 67:178–188. https://doi.org/10.1016/j.plaphy.2013.03.004
Duarte B, Valentim JM, Dias JM et al (2014b) Modelling sea level rise (SLR) impacts on salt marsh detrital outwelling C and N exports from an estuarine coastal lagoon to the ocean (Ria de Aveiro, Portugal). Ecol Model 289:36–44. https://doi.org/10.1016/j.ecolmodel.2014.06.020
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963. https://doi.org/10.1111/j.1469-8137.2008.02531.x
Fonseca VF, França S, Duarte B et al (2019) Spatial variation in mercury bioaccumulation and magnification in a temperate estuarine food web. Front Mar Sci 6:117. https://doi.org/10.3389/fmars.2019.00117
Freeman C, Ostle NJ, Fenner N, Kang H (2004) A regulatory role for phenol oxidase during decomposition in peatlands. Soil Biol Biochem 36:1663–1667. https://doi.org/10.1016/j.soilbio.2004.07.012
Freitas J, Duarte B, Caçador I (2014) Biogeochemical drivers of phosphatase activity in salt marsh sediments. J Sea Res 93:57–62. https://doi.org/10.1016/j.seares.2014.04.002
Ge Z-M, Guo H-Q, Zhao B, Zhang L-Q (2015) Plant invasion impacts on the gross and net primary production of the salt marsh on eastern coast of China: insights from leaf to ecosystem. J Geophys Res Biogeosci 120:169–186. https://doi.org/10.1002/2014JG002736
Geraldi NR, Ortega A, Serrano O et al (2019) Fingerprinting blue carbon: rationale and tools to determine the source of organic carbon in marine depositional environments. Front Mar Sci 6:1–9. https://doi.org/10.3389/fmars.2019.00263
He Q, Wu Y, Bing H et al (2020) Vegetation type rather than climate modulates the variation in soil enzyme activities and stoichiometry in subalpine forests in the eastern Tibetan Plateau. Geoderma 374:114424. https://doi.org/10.1016/j.geoderma.2020.114424
Himes-Cornell A, Pendleton L, Atiyah P (2018) Valuing ecosystem services from blue forests: a systematic review of the valuation of salt marshes, sea grass beds and mangrove forests. Ecosyst Serv 30:36–48. https://doi.org/10.1016/j.ecoser.2018.01.006
Huang L, Zhang Y, Shi Y et al (2015) Comparison of phosphorus fractions and phosphatase activities in coastal wetland soils along vegetation zones of Yancheng National Nature Reserve, China. Estuar Coast Shelf Sci 157:93–98. https://doi.org/10.1016/j.ecss.2014.09.027
Huang X, Morris JT (2005) Distribution of phosphatase activity in marsh sediments along an estuarine salinity gradient. Mar Ecol Prog Ser 292:75–83. https://doi.org/10.3354/meps292075
Human LRD, Feijão E, Cruz de Carvalho R et al (2020) Mediterranean salt marsh sediment metal speciation and bioavailability changes induced by the spreading of non-indigenous Spartina patens. Estuar Coast Shelf Sci 243:106921. https://doi.org/10.1016/j.ecss.2020.106921
Kazemi K, Zhang B, Lye LM (2017) Assessment of microbial communities and their relationship with enzymatic activity during composting. World J Eng Technol 5:93–102. https://doi.org/10.4236/wjet.2017.53B011
Kelley AM, Fay PA, Polley HW, et al (2011) Atmospheric CO2 and soil extracellular enzyme activity: a meta-analysis and CO2 gradient experiment. Ecosphere 2:art96. https://doi.org/10.1890/ES11-00117.1
Ladd JN, Brisbane PG, Butler JHA, Amato M (1976) Studies on soil fumigation—III: effects on enzyme activities, bacterial numbers and extractable ninhydrin reactive compounds. Soil Biol Biochem 8:255–260. https://doi.org/10.1016/0038-0717(76)90053-5
Li B, Liao C, Zhang X et al (2009) Spartina alterniflora invasions in the Yangtze River estuary, China: an overview of current status and ecosystem effects. Ecol Eng 35:511–520. https://doi.org/10.1016/j.ecoleng.2008.05.013
Li Y, Sun L-L, Sun Y-Y, et al (2019) Extracellular enzyme activity and its implications for organic matter cycling in northern Chinese marginal seas. Frontiers in Microbiology 10:
Lillebø AI, Flindt MR, Pardal MÂ, Marques JC (1999) The effect of macrofauna, meiofauna and microfauna on the degradation of Spartina maritima detritus from a salt marsh area. Acta Oecologica 20:249–258. https://doi.org/10.1016/S1146-609X(99)00141-1
Lin Q, Mendelssohn IA (2008) Determining tolerance limits for restoration and phytoremediation with Spartina patens in crude oil-contaminated sediment in greenhouse. Arch Agron Soil Sci 54:681–690. https://doi.org/10.1080/03650340802253937
Megonigal JP, Neubauer SC (2019) Chapter 19 - biogeochemistry of tidal freshwater wetlands. In: Perillo GME, Wolanski E, Cahoon DR, Hopkinson CS (eds) Coastal Wetlands. Elsevier, pp 641–683
Menon R, Jackson CR, Holland MM (2013) The influence of vegetation on microbial enzyme activity and bacterial community structure in freshwater constructed wetland sediments. Wetlands 33:365–378. https://doi.org/10.1007/s13157-013-0394-0
Mucha AP, Almeida CMR, Bordalo AA, Vasconcelos MTSD (2008) Salt marsh plants (Juncus maritimus and Scirpus maritimus) as sources of strong complexing ligands. Estuar Coast Shelf Sci 77:104–112. https://doi.org/10.1016/j.ecss.2007.09.011
Mucha AP, Almeida CMR, Bordalo AA, Vasconcelos MTSD (2010) LMWOA (low molecular weight organic acid) exudation by salt marsh plants: natural variation and response to Cu contamination. Estuar Coast Shelf Sci 88:63–70. https://doi.org/10.1016/j.ecss.2010.03.008
Newell SY (1993) Decomposition of shoots of a salt-marsh grass. In: Jones JG (ed) Advances in microbial ecology. Springer, Boston, pp 301–326
Nordström MC, Currin CA, Talley TS et al (2014) Benthic food-web succession in a developing salt marsh. Mar Ecol Prog Ser 500:43–55. https://doi.org/10.3354/meps10686
Paredes-Páliz K, Rodríguez-Vázquez R, Duarte B et al (2018) Investigating the mechanisms underlying phytoprotection by plant growth-promoting rhizobacteria in Spartina densiflora under metal stress. Plant Biol 20:497–506. https://doi.org/10.1111/plb.12693
Pereira P, Caçador I, Vale C et al (2007) Decomposition of belowground litter and metal dynamics in salt marshes (Tagus Estuary, Portugal). Sci Total Environ 380:93–101. https://doi.org/10.1016/j.scitotenv.2007.01.056
Ravit B, Ehrenfeld JG, Haggblom MM (2003) A comparison of sediment microbial communities associated withPhragmites australis andSpartina alterniflora in two brackish wetlands of New Jersey. Estuaries 26:465–474. https://doi.org/10.1007/BF02823723
Rietl AJ, Overlander ME, Nyman AJ, Jackson CR (2016) Microbial community composition and extracellular enzyme activities associated with juncus roemerianus and spartina alterniflora vegetated sediments in louisiana saltmarshes. Microb Ecol 71:290–303. https://doi.org/10.1007/s00248-015-0651-2
SanLeon DG, Izco J, Sánchez JM (1999) Spartina patensas a weed in Galician saltmarshes (NW Iberian Peninsula). Hydrobiologia 415:213–222
Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404. https://doi.org/10.1016/j.soilbio.2009.10.014
Sousa AI, Lillebø AI, Caçador I, Pardal MA (2008) Contribution of Spartina maritima to the reduction of eutrophication in estuarine systems. Environ Pollut 156:628–635. https://doi.org/10.1016/j.envpol.2008.06.022
Sousa AI, Lillebø AI, Pardal MA, Caçador I (2010) Productivity and nutrient cycling in salt marshes: contribution to ecosystem health. Estuar Coast Shelf Sci 87:640–646. https://doi.org/10.1016/j.ecss.2010.03.007
Sousa AI, Lillebø AI, Risgaard-Petersen N et al (2012) Denitrification: an ecosystem service provided by salt marshes. Mar Ecol Prog Ser 448:79–92. https://doi.org/10.3354/meps09526
Stewart GR, Lee JA, Orebamjo TO (1972) Nitrogen metabolism of halophytes. New Phytol 71:263–267. https://doi.org/10.1111/j.1469-8137.1972.tb04072.x
Strong DR, Ayres DR (2013) Ecological and evolutionary misadventures of spartina. Annu Rev Ecol Evol Syst 44:389–410. https://doi.org/10.1146/annurev-ecolsys-110512-135803
Tabak HH, Lens P, van Hullebusch ED, Dejonghe W (2005) Developments in bioremediation of soils and sediments polluted with metals and radionuclides – 1. microbial processes and mechanisms affecting bioremediation of metal contamination and influencing metal toxicity and transport. Rev Environ Sci Biotechnol 4:115–156. https://doi.org/10.1007/s11157-005-2169-4
Talbi Zribi O, Mbarki S, Hamdi A, Abdelly C (2020) Physiological responses of halophytes to the combined effects of salinity and phosphorus deficiency. In: Grigore M-N (ed) Handbook of halophytes: from molecules to ecosystems towards biosaline agriculture. Springer International Publishing, Cham, pp 1–17
Tobias C, Neubauer SC (2019) Chapter 16 - salt marsh biogeochemistry—An overview. In: Perillo GME, Wolanski E, Cahoon DR, Hopkinson CS (eds) Coastal wetlands. Elsevier, pp 539–596
Valiela I, Teal JM, Allen SD et al (1985) Decomposition in salt marsh ecosystems: the phases and major factors affecting disappearance of above-ground organic matter. J Exp Mar Biol Ecol 89:29–54. https://doi.org/10.1016/0022-0981(85)90080-2
van Hullebusch ED, Lens PNL, Tabak HH (2005) Developments in bioremediation of soils and sediments polluted with metals and radionuclides. 3. influence of chemical speciation and bioavailability on contaminants immobilization/mobilization bio-processes. Rev Environ Sci Biotechnol 4:185–212. https://doi.org/10.1007/s11157-005-2948-y
Vera F, Gutiérrez JL, Ribeiro PD (2009) Aerial and detritus production of the cordgrass Spartina densiflora in a southwestern Atlantic salt marsh. Botany 87:482–491. https://doi.org/10.1139/B09-017
Wallenius K, Rita H, Simpanen S et al (2010) Sample storage for soil enzyme activity and bacterial community profiles. J Microbiol Methods 81:48–55. https://doi.org/10.1016/j.mimet.2010.01.021
Windham L, Ehrenfeld JG (2003) Net impact of a plant invasion on nitrogen-cycling processes within a brackish tidal marsh. Ecol Appl 13:883–896. https://doi.org/10.1890/02-5005
Windham L, Weis JS, Weis P (2004) Metal dynamics of plant litter of Spartina alterniflora and Phragmites australis in metal-contaminated salt marshes. Part 1: patterns of decomposition and metal uptake. Environ Toxicol Chem 23:1520–1528. https://doi.org/10.1897/03-284
Wu J, Seliskar DM, Gallagher JL (1998) Stress tolerance in the marsh plant Spartina patens: Impact of NaCl on growth and root plasm membrane lipid composition. Physiol Plant 102:307–317
Wu Y, Leng Z, Li J et al (2021) Sulfur mediated heavy metal biogeochemical cycles in coastal wetlands: from sediments, rhizosphere to vegetation. Front Environ Sci Eng 16:102. https://doi.org/10.1007/s11783-022-1523-x
Zhong-Yi C, Bo LI, Jia-Kuan C (2004) Ecological consequences and management of Spartina spp. invasions in coastal ecosystems. Biodiversity Science, 12:280. https://doi.org/10.17520/biods.2004034
zu Ermgassen PSE, Baker R, Beck MW et al (2021) Ecosystem services: delivering decision-making for salt marshes. Estuar Coasts 44:1691–1698. https://doi.org/10.1007/s12237-021-00952-z
Funding
The authors would like to thank Fundação para a Ciência e a Tecnologia (FCT) for funding MARE—Marine and Environmental Sciences Centre (UIDP/04292/2020 and UIDB/04292/2020), ARNET—Aquatic Research Infrastructure Network Associated Laboratory (LA/P/0069/2020). Work was also funded by MAR 2020 program via the Project RESTAURA2020 (16-01-04-FMP-0014). B. Duarte and V. F. Fonseca were supported by investigation contracts (CEECIND/00511/2017, DL57/2016/CP1479/CT0024 and 2021.00244.CEECIND).
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Duarte, B., Fonseca, V.F., Reis-Santos, P. et al. Bioinvasion by Spartina patens alters sediment biogeochemical functioning of European salt marshes. Biol Invasions 24, 3217–3232 (2022). https://doi.org/10.1007/s10530-022-02841-3
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DOI: https://doi.org/10.1007/s10530-022-02841-3