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Silver nanoparticles intensify the allelopathic intensity of four invasive plant species in the Asteraceae

Abstract

This study aimed to estimate the allelopathic intensity of four Asteraceae invasive plant species (IPS), including Conyza canadensis (L.) Cronq., Erigeron annuus (L.) Pers., Bidens pilosa (L.), and Aster subulatus Michx., by testing the effect of leaf extracts on the seed germination and seedling growth (SGe and SGr) of lettuce (Lactuca sativa L.) in combination with two particle sizes of silver nanoparticles. These four IPS decreased the germination of lettuce seeds but increased the growth of lettuce seedlings. The allelopathic intensity of the four IPS decreased in the following order: B. pilosa > C. canadensis > E. annuus > A. subulatus. Silver nanoparticles decreased the SGe and SGr of lettuce. The 20 nm silver nanoparticles affected the competition intensity for water and the absorption of inorganic salts by lettuce more intensively than the 80 nm nanoparticles. Silver nanoparticles intensify the allelopathic intensity of the four invasive plant species on the SGe and SGr of lettuce. The allelopathic intensity of B. pilosa was higher than that of the other three IPS when they were polluted with silver nanoparticles. Thus, silver nanoparticles could facilitate the invasion process of the four IPS, particularly B. pilosa, via an increase in the intensity of allelopathy.

Key words
Ag ion; allelochemicals; invasion process; lettuce; particle size

INTRODUCTION

Invasive plant species have a noticeable impact on the composition and structure of the habitats that they encroach upon, and, in particular, those invaders can lead to a loss of biodiversity (Wang et al. 2018aWANG CY, JIANG K, LIU J, ZHOU JW WU BD. 2018a. Moderate and heavy Solidago canadensis L. invasion are associated with decreased taxonomic diversity but increased functional diversity of plant communities in East China. Ecol Eng 112: 55-64., bWANG CY, JIANG K, ZHOU JW WU BD. 2018b. Solidago canadensis invasion affects soil N-fixing bacterial communities in heterogeneous landscapes in urban ecosystems in East China. Sci Total Environ 631-632: 702-713., 2019aWANG CY, WU BD, JIANG K, ZHOU JW, LIU J LV YN. 2019a. Canada goldenrod invasion cause significant shifts in the taxonomic diversity and community stability of plant communities in heterogeneous landscapes in urban ecosystems in East China. Ecol Eng 127: 504-509.-cWANG S, WEI M, WU BD, JIANG K, DU DL WANG CY. 2019c. Degree of invasion of Canada goldenrod (Solidago canadensis L.) plays an important role in the variation of plant taxonomic diversity and community stability in eastern China. Ecol Res 34: 782-789., 2020aWANG CY, WEI M, WANG S, WU BD CHENG HY. 2020a. Erigeron annuus (L.) Pers. and Solidago canadensis L. antagonistically affect community stability and community invasibility under the co-invasion condition. Sci Total Environ 716: 137128., bWANG CY, WEI M, WANG S, WU BD DU DL. 2020b. Cadmium influences the litter decomposition of Solidago canadensis L. and soil N-fixing bacterial communities. Chemosphere 246: 125717., 2021WANG CY, CHENG HY, WU BD, JIANG K, WANG S, WEI M DU DL. 2021. The functional diversity of native ecosystems increases during the major invasion by the invasive alien species, Conyza canadensis. Ecol Eng 159: 106093., Wu et al. 2019aWU BD, WANG L, WEI M, WANG S, JIANG K WANG CY. 2019b. Silver nanoparticles reduced the invasiveness of redroot pigweed. Ecotoxicology 28: 983-994., Wei et al. 2020aWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020a. Heavy metal pollution improves allelopathic effects of Canada goldenrod on lettuce germination. Plant Biol 22: 832-838., b). Thus, the mechanisms that lead to the successful invasion by invasive plant species are currently one of the main topics of study on the ecological effects of invasive plant species. In particular, the new weapon hypothesis verifies that numerous invasive plant species can incur evident allelopathic intensity by secreting several types of secondary substances and noxious compounds, i.e., allelochemicals, that can decrease the growth of native plants (Djurdjević et al. 2012DJURDJEVIĆ L, GAJIĆ G, KOSTIĆ O, JARIĆ S, PAVLOVIĆ M, MITROVIĆ M PAVLOVIĆ P. 2012. Seasonal dynamics of allelopathically significant phenolic compounds in globally successful invader Conyza canadensis L. plants and associated sandy soil. Flora 207: 812-820., Fabbro et al. 2014FABBRO CD, GÜSEWELL S PRATI D. 2014. Allelopathic effects of three plant invaders on germination of native species: a field study. Biol Invasions 16: 1035-1042., Lyytinen & Lindström 2019LYYTINEN A LINDSTRÖM L. 2019. Responses of a native plant species from invaded and uninvaded areas to allelopathic effects of an invader. Ecol Evol 9: 6116-6123., Hsueh et al. 2020HSUEH MT, FAN CH CHANG WL. 2020. Allelopathic effects of Bidens pilosa L. var. radiata Sch. Bip. on the tuber sprouting and seedling growth of Cyperus rotundus L. Plants 9: 742., Wei et al. 2020aWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020a. Heavy metal pollution improves allelopathic effects of Canada goldenrod on lettuce germination. Plant Biol 22: 832-838., b). More importantly, the process of seed germination and seedling growth (SGe and SGr) was most obviously affected by the allelochemicals of invasive plant species at the beginning of their life history (Fabbro et al. 2014FABBRO CD, GÜSEWELL S PRATI D. 2014. Allelopathic effects of three plant invaders on germination of native species: a field study. Biol Invasions 16: 1035-1042., Wang et al. 2017aWANG CY, JIANG K, ZHOU JW LIU J. 2017a. Allelopathic suppression by Conyza canadensis depends on the interaction between latitude and the degree of the plant’s invasion. Acta Bot Bras 31: 212-219., bWANG CY, ZHOU JW, JIANG K LIU J. 2017b. Differences in leaf functional traits and allelopathic effects on seed germination and growth of Lactuca sativa between red and green leaves of Rhus typhina. South Afr J Bot 111: 17-22., 2018cWANG CY, JIANG K, WU BD, ZHOU JW LV YN. 2018c. Silver nanoparticles with different particle sizes enhance the allelopathic effects of Canada goldenrod on the seed germination and seedling development of lettuce. Ecotoxicology 27: 1116-1125., dWANG CY, JIANG K, WU BD ZHOU JW. 2018d. The combined treatments of Canada goldenrod leaf extracts and Cadmium pollution confer an inhibitory effect on seed germination and seedling development of lettuce. Aust J Bot 66: 331-337., 2019dWANG CY, WU BD JIANG K. 2019d. Allelopathic effects of Canada goldenrod leaf extracts on the seed germination and seedling growth of lettuce reinforced under salt stress. Ecotoxicology 28: 103-116., 2020cWANG S, WEI M, WU BD, CHENG HY WANG CY. 2020c. Combined nitrogen deposition and Cd stress antagonistically affect the allelopathy of invasive alien species Canada goldenrod on the cultivated crop lettuce. Sci Horticul 261: 108955., Carvalhoa et al. 2019CARVALHOA MSS, ANDRADE-VIEIRA LF, DOS SANTOS FE, CORREA FF, DAS GRAÇAS CARDOSO M VILELA LR. 2019. Allelopathic potential and phytochemical screening of ethanolic extracts from five species of Amaranthus spp. in the plant model Lactuca sativa. Sci Hortic 245: 90-98., Hsueh et al. 2020HSUEH MT, FAN CH CHANG WL. 2020. Allelopathic effects of Bidens pilosa L. var. radiata Sch. Bip. on the tuber sprouting and seedling growth of Cyperus rotundus L. Plants 9: 742., Krstin et al. 2021KRSTIN L, KATANI Z, PFEIFFER TŽ, MARONIĆ DŠ, MARINČIĆ D, MARTINOVIĆ A ČAMAGAJEVAC IŠ. 2021. Phytotoxic effect of invasive species Amorpha fruticosa L. on germination and the early growth of forage and agricultural crop plants. Ecol Res 36: 97-106.). However, SGe and SGr are critical to individual growth and the development of biomes. Thus, the allelopathic intensity of invasive plant species on the SGe and SGr of natives can decrease the competitive intensity of their growth (Wang et al. 2018c, d, 2019d, 2020c, Carvalhoa et al. 2019CARVALHOA MSS, ANDRADE-VIEIRA LF, DOS SANTOS FE, CORREA FF, DAS GRAÇAS CARDOSO M VILELA LR. 2019. Allelopathic potential and phytochemical screening of ethanolic extracts from five species of Amaranthus spp. in the plant model Lactuca sativa. Sci Hortic 245: 90-98., Wei et al. 2020aWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020a. Heavy metal pollution improves allelopathic effects of Canada goldenrod on lettuce germination. Plant Biol 22: 832-838., b, Krstin et al. 2021KRSTIN L, KATANI Z, PFEIFFER TŽ, MARONIĆ DŠ, MARINČIĆ D, MARTINOVIĆ A ČAMAGAJEVAC IŠ. 2021. Phytotoxic effect of invasive species Amorpha fruticosa L. on germination and the early growth of forage and agricultural crop plants. Ecol Res 36: 97-106.). Moreover, the Asteraceae is the plant family with the highest number of invasive plant species in China (Wang et al. 2016WANG CY, LIU J, XIAO HG, ZHOU JW DU DL. 2016. Floristic characteristics of alien invasive seed plant species in China. An Acad Bras Cienc 88: 1791-1797.). Thus, it is necessary to analyze the allelopathic intensity recruited by invasive plant species in the Asteraceae on the SGe and SGr of natives to obtain a better explanation for the mechanisms that lead to the successful invasion of invasive plant species.

In addition, drivers of the shifts in SGe and SGr beyond the allelopathic intensity created by invasive plant species may presumably mediate a momentous effect on this aspect. Subsequently, the process of plant invasion and its associated ecological effects may be changed or even made more complex under the interaction of one of these drivers. As one of the most widely used nanomaterials, a substantial amount of silver nanoparticles has been released into the environment and totals 500 tons a year across the globe. These nanomaterials are primarily derived from their production and use in a number of industries, including catalysts, optics, electronics, cosmetics, medicine, pharmaceuticals, and food (McGillicuddy et al. 2017MCGILLICUDDY E, MURRAY I, KAVANAGH S, MORRISON L, FOGARTY A, CORMICAN M, DOCKERY P, PRENDERGAST M, ROWAN N MORRIS D. 2017. Silver nanoparticles in the environment: Sources, detection and ecotoxicology. Sci Total Environ 575: 231-246., Wu et al. 2019bWU BD, ZHANG HS, JIANG K, ZHOU JW WANG CY. 2019a. Erigeron canadensis affects the taxonomic and functional diversity of plant communities in two climate zones in the North of China. Ecol Res 34: 535-547., Wang et al. 2020dWANG S, WU BD, WEI M, ZHOU JW, JIANG K WANG CY. 2020d. Silver nanoparticles with different concentrations and particle sizes affect the functional traits of wheat. Biol Plantarum 64: 1-8.). However, the silver nanoparticles that are released end up in the soil subsystem and then cause ecotoxicological effects over a long period, particularly via the food cycle (McGillicuddy et al. 2017MCGILLICUDDY E, MURRAY I, KAVANAGH S, MORRISON L, FOGARTY A, CORMICAN M, DOCKERY P, PRENDERGAST M, ROWAN N MORRIS D. 2017. Silver nanoparticles in the environment: Sources, detection and ecotoxicology. Sci Total Environ 575: 231-246., Wu et al. 2019bWU BD, ZHANG HS, JIANG K, ZHOU JW WANG CY. 2019a. Erigeron canadensis affects the taxonomic and functional diversity of plant communities in two climate zones in the North of China. Ecol Res 34: 535-547., Wang et al. 2020d). Predictably, silver nanoparticles will be released into the environment in the future with the increasing frequency and intensity of anthropogenic activities, particularly as the industry develops further. In particular, the increasing level of pollution mediated by silver nanoparticles can pose an obvious effect on the invasion process and the underlying mechanisms of invasive plant species (Wang et al. 2018c, Wu et al. 2019bWU BD, ZHANG HS, JIANG K, ZHOU JW WANG CY. 2019a. Erigeron canadensis affects the taxonomic and functional diversity of plant communities in two climate zones in the North of China. Ecol Res 34: 535-547.). Therefore, it is vital to understand the allelopathic intensity of the Asteraceae invasive plant species on the SGe and SGr of natives that are affected by silver nanoparticles. Previous studies largely focused on the allelopathic intensity of only one invasive plant species on the SGe and SGr of natives. However, research on the allelopathic intensity of a variety of invasive plant species on the SGe and SGr of natives, particularly under silver nanoparticles, is limited.

This study aimed to estimate the allelopathic intensity of the notorious four invasive plant species of the Asteraceae, i.e., Conyza canadensis (L.) Cronq., Erigeron annuus (L.) Pers., Bidens pilosa (L.), and Aster subulatus Michx., on the seed germination and seedling growth of lettuce (Lactuca sativa L.) after exposure to 20 nm and 80 nm particle sizes of silver nanoparticles. In particular, the four Asteraceae invasive plant species originated in North America, and therefore, they may share a similar or even the same evolutionary history during their colonization and invasion in China (Wang et al. 2016WANG CY, LIU J, XIAO HG, ZHOU JW DU DL. 2016. Floristic characteristics of alien invasive seed plant species in China. An Acad Bras Cienc 88: 1791-1797.). Furthermore, the four Asteraceae invasive plant species are currently considered to be the most harmful invasive plant species in China owing to their notable influence on native plant communities. Additionally, farmlands and wastelands are more vulnerable to the process of invasion of the four Asteraceae invasive plant species in China. In addition, the allelopathic intensity of the four Asteraceae invasive plant species on the SGe and SGr of native ones is a vital issue in their successful invasion (Khanh et al. 2009KHANH TD, CONG LC, XUAN TD, UEZATO Y, DEBA F, TOYAMA T TAWATA S. 2009. Allelopathic plants: 20. Hairy beggarticks (Bidens pilosa L.). Allelopathy J 24: 243-254., Djurdjević et al. 2012DJURDJEVIĆ L, GAJIĆ G, KOSTIĆ O, JARIĆ S, PAVLOVIĆ M, MITROVIĆ M PAVLOVIĆ P. 2012. Seasonal dynamics of allelopathically significant phenolic compounds in globally successful invader Conyza canadensis L. plants and associated sandy soil. Flora 207: 812-820., Fabbro et al. 2014FABBRO CD, GÜSEWELL S PRATI D. 2014. Allelopathic effects of three plant invaders on germination of native species: a field study. Biol Invasions 16: 1035-1042., Wang et al. 2017a, He et al. 2019HE P, DENG YJ, HU XY, HU XY, PAN HM DENG HP. 2019. Potential allelopathic effect of Aster subulatus on Triticum aestivum and Brassica chinensis. Acta Pratacul Sin 28: 101-109., Hsueh et al. 2020HSUEH MT, FAN CH CHANG WL. 2020. Allelopathic effects of Bidens pilosa L. var. radiata Sch. Bip. on the tuber sprouting and seedling growth of Cyperus rotundus L. Plants 9: 742., Lu et al. 2020LU YJ, WANG YF, WU BD, WANG S, WEI M, DU DL WANG CY. 2020. Allelopathy of three Compositae invasive alien species on indigenous Lactuca sativa L. enhanced under Cu and Pb pollution. Sci Hortic 267: 109323., Wei et al. 2020bWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020b. Combined allelopathy of Canada goldenrod and horseweed on the seed germination and seedling growth performance of lettuce. Landsc Ecol Eng 16: 299-306.). Moreover, as one of the most frequent native species in the environments occupied by the four Asteraceae invasive plant species, lettuce seedlings are highly sensitive to stress in the environment. Therefore, the growth of lettuce seedlings is more sensitive to the allelopathic intensity of invasive plant species on the SGe and SGr of natives (Khanh et al. 2009KHANH TD, CONG LC, XUAN TD, UEZATO Y, DEBA F, TOYAMA T TAWATA S. 2009. Allelopathic plants: 20. Hairy beggarticks (Bidens pilosa L.). Allelopathy J 24: 243-254., Wang et al. 2017a, b, 2018c, d, 2019d, 2020c, Carvalhoa et al. 2019CARVALHOA MSS, ANDRADE-VIEIRA LF, DOS SANTOS FE, CORREA FF, DAS GRAÇAS CARDOSO M VILELA LR. 2019. Allelopathic potential and phytochemical screening of ethanolic extracts from five species of Amaranthus spp. in the plant model Lactuca sativa. Sci Hortic 245: 90-98., Wei et al. 2020aWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020a. Heavy metal pollution improves allelopathic effects of Canada goldenrod on lettuce germination. Plant Biol 22: 832-838., b). In addition, the four Asteraceae invasive plant species and lettuce can co-exist in the same habitat, particularly in the farmlands and wildlands. Lastly, the four Asteraceae invasive plant species and lettuce belong to the Asteraceae, which currently contains the largest number of invasive plant species of any family of plants in China (Wang et al. 2016WANG CY, LIU J, XIAO HG, ZHOU JW DU DL. 2016. Floristic characteristics of alien invasive seed plant species in China. An Acad Bras Cienc 88: 1791-1797.).

Table I
Summary of experimental design.

We present the following hypotheses: (I) the four Asteraceae invasive plant species can create intensive allelopathic intensity on lettuce the SGe and SGr of lettuce, and there may be remarkable differences in the allelopathic intensity of these invasive plant species on lettuce; (II) silver nanoparticles can reduce the SGe and SGr of lettuce, and silver nanoparticles that are 20 nm tend to more toxic than that are 80 nm; and (III) silver nanoparticles can intensify the allelopathic intensity of the four Asteraceae invasive plant species on lettuce SGe and SGr.

MATERIALS AND METHODS

Preparation of plant materials and allelopathic solutions

Fully mature leaves samples of the four Asteraceae invasive plant species, including C. canadensis, E. annuus, B. pilosa, and A. subulatus, were randomly collected from Zhenjiang, Jiangsu (32.21°N, 119.52°E), China in the middle of September 2019. Zhenjiang has a subtropical monsoon humid climate (annual mean precipitation: ≈ 1,101.4 mm; annual mean temperature: ≈ 15.9°C; annual mean hours of sunshine: ≈ 1,996.8 h) (Jia & Wu 2020JIA S WU HP. 2020. Zhenjiang Yearbook: Overview of Zhenjiang. Organized by Zhenjiang Municipal People’s Government Written by Zhenjiang Local Records Office. In: Yu W, Ye ZG, Sun WY, Yang ZH, Zong CJ, Qian JJ Pan Y (Eds). Publishing House of Local Records, Beijing, p. 14-15.). The harvested leaves of the four Asteraceae invasive plant species were moderately washed and then thoroughly air-dried at approximately 25 °C. The air-dried leaves of the four Asteraceae invasive plant species were then soaked using sterile distilled water in the flasks at approximately 25 °C to yield the allelopathic solution (20 g L−1). This concentration was used to simulate the plants that were subjected to the growth of invasive plant species. In contrast, undisturbed wild growth was simulated using distilled water as the control (CK, 0 mg L–1). The allelopathic solution was stored at 4°C for less than a week.

Preparation of the silver nanoparticles solutions

Solutions with silver nanoparticles of two particle sizes, 20 nm and 80 nm, were prepared using AgNP (purity ≥99.9%). Silver nanoparticles of 20 nm and 80 nm are widely used in the study area. A silver nanoparticles solution with 20 nm and one with 80 nm were all established at 100 mg L–1, which is comparable to the concentrations found in soils polluted with silver nanoparticles. Distilled water was used as the control (0 mg L–1), and it simulated soil that had not been polluted with silver nanoparticles pollution. In particular, a AgNP solution was homogenized by stirring with an ultrasonoscope (Q-250DE) at 25 °C at approximately 40 kHz with its strongest power at 100 W for approximately 4 h to sufficiently disperse the particles to avoid the accumulation of silver nanoparticles (Wang et al. 2018c, 2020d, Wu et al. 2019bWU BD, ZHANG HS, JIANG K, ZHOU JW WANG CY. 2019a. Erigeron canadensis affects the taxonomic and functional diversity of plant communities in two climate zones in the North of China. Ecol Res 34: 535-547.).

Experimental design of lettuce seed germination and seedling growth

The experiment comprised 15 treatments with all independent or mixed treatments of an allelopathic solution of the four Asteraceae invasive plant species and silver nanoparticles solutions that were 20 or 80 nm. The information of the experimental design is defined in Table I.

Lettuce seeds (the cultivar: Lactuca sativa L. cv. Kexing-Jiuzhouhong) were hydroponically cultured in Petri dishes (9 cm in diameter) from October 10 to 18, 2019. The lettuce seeds were surface-sterilized using 1% NaClO for approximately 15 min. The surface-sterilized lettuce seeds were then cleaned carefully using sterile deionized water. The washed lettuce seeds were then carefully moved to Petri dishes with 30 seeds per Petri dish. Two layers of filter paper were enclosed under the lettuce seeds in each dish. The cultured lettuce seeds in the Petri dishes were placed in an electronic-controlled incubator (LRH-250-G) with 27.5 µmol m–2 s–1 (12 h of alternating light and dark per day) at approximately 25°C. On the first day, 5 mL of deionized water was used to soak the lettuce seedlings and the filter paper. After that, 0.5 mL of sterile deionized water, the allelopathic solution of the four Asteraceae, and/or a solution of AgNPs were added to each Petri dish daily using a pipette (Eppendorf Research® Plus). The number of germinated lettuce seeds, measured by exposure of the radicle, was recorded daily (Wang et al. 2017a, 2018c, d, 2019d, Wei et al. 2020bWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020b. Combined allelopathy of Canada goldenrod and horseweed on the seed germination and seedling growth performance of lettuce. Landsc Ecol Eng 16: 299-306.). Three Petri dishes were utilized per treatment.

Determination of lettuce seed germination and seedling growth indices

After 8 d, 10 lettuce seedlings per Petri dish, i.e., three Petri dishes per treatment * 10 seedlings per Petri dish for determination (with 30 seeds per Petri dish for germination) = 30 seedlings per treatment for determination, were randomly selected to assess the values of lettuce SGe and SGr indices. In particular, the germination percentage was calculated as the ratio of the number of the germinated seeds to the total number of the tested seeds and denotes the germination capacity. The germination potential was calculated as the germination percentage after 3 d of cultivation and denotes the germination intensity and homogeneity. The germination index was calculated as the following equation: germination index = Gi /Dt , where Gi is the number of the germinated seeds in Dt , i.e., the time after cultivation (day), which denotes germination power. The germination rate index was calculated as the arithmetic product of the two values of germination percentage and germination index and denotes germination rate and vitality. The germination vigor index was calculated as the arithmetic product of the two values of germination index and seedling fresh weight and denotes germination rate and vitality. The promptness index was calculated as the following equation: (1.00) * nd2 + (0.75) * nd4 + (0.50) * nd6 + (0.25) * nd8, where nd2, nd4, nd6, nd8 are the number of the germinated seeds in the second, fourth, sixth, and eighth days after cultivation, respectively, and denotes the response capability of seed germination. The seedling height, which indicates the distance between the base of the stem and the apical shoot, was measured by a ruler that was accurate down to 0.1 cm and denotes the competitive intensity for sunlight capture. The root length was the distance between the base of the root and the root tip and was measured by a ruler that was accurate to 0.1 cm; it denotes the competitive intensity for water and the absorption of inorganic salts. The leaf length was considered to be the maximum value parallel with the midrib, which was measured by a ruler that was accurate to 0.1 cm, and denotes the competitive intensity for sunlight capture. The leaf width, which is the maximum value perpendicular to the midrib, was measured by a ruler with 0.1 cm accuracy and denotes the competitive intensity for the capture of sunlight. The green leaf area was calculated as the following equation: the green leaf area = 0.75 × leaf length × leaf width, which denotes the photosynthetic area. The seedling biomass, which includes the fresh and dry weight, was estimated by an electronic balance with an accuracy of 0.001 g and denotes the growing competitive intensity. The moisture content was calculated as the ratio of the difference between the seedling fresh weight and the seedling dry weight to the seedling fresh weight and denotes the water content (Steinmaus et al. 2000STEINMAUS SJ, TIMONTHY SP JODIE SH. 2000. Estimation of base temperature for nine weed species. J Exp Bot 51: 275-286., Toscano et al. 2017TOSCANO S, ROMANO D, TRIBULATO A PATANE C. 2017. Effects of drought stress on seed germination of ornamental sunflowers. Acta Physiol Plant 39: 184., Ding et al. 2018DING TL, YANG Z, WEI XC, YUAN F, YIN SS WANG BS. 2018. Evaluation of salt-tolerant germplasm and screening of the salt-tolerance traits of sweet sorghum in the germination stage. Plant Species Biol 45: 1073-1081., Huang et al. 2018HUANG SS, SUN, LQ, HU, X, WANG YH, ZHANG YJ, NEVO E, PENG JH SUN DF. 2018. Associations of canopy leaf traits with SNP markers in durum wheat (Triticum turgidum L. durum (Desf.)). PLoS ONE 13: e206226., Wang et al. 2018c, 2019d, 2020eWANG S, WEI M, CHENG HY, WU BD, DU DL WANG CY. 2020e. Indigenous plant species and invasive alien species tend to diverge functionally under heavy metal pollution and drought stress. Ecotox Environ Safe 205: 111160., Lu et al. 2020LU YJ, WANG YF, WU BD, WANG S, WEI M, DU DL WANG CY. 2020. Allelopathy of three Compositae invasive alien species on indigenous Lactuca sativa L. enhanced under Cu and Pb pollution. Sci Hortic 267: 109323., Wei et al. 2020bWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020b. Combined allelopathy of Canada goldenrod and horseweed on the seed germination and seedling growth performance of lettuce. Landsc Ecol Eng 16: 299-306.).

Statistical analyses

Differences in the lettuce SGe and SGr indices among all treatments were estimated using a one-way analysis of variance (ANOVA) with a Tukey’s test. P ≤ 0.05 was defined as the threshold for statistical significance. The statistical analyses were completed using IBM SPSS Statistics 25.0 (IBM, Inc., Armonk, NY, USA).

RESULTS

Influence of the allelopathic intensity of the four asteraceae invasive plant species on lettuce seed germination and seedling growth compared with the CK

The germination percentage, germination index, germination vigor index, and promptness index of lettuce decreased, but the green leaf area, leaf length, moisture content, fresh weight, and seedling height of lettuce increased under CC (P < 0.05; Figs. 1 and 2). The germination index, germination vigor index, promptness index, and root length of lettuce decreased, but the green leaf area and leaf length of lettuce increased under EA (P < 0.05; Figs. 1 and 2). The germination index, germination potential, germination rate index, germination vigor index, promptness index, root length, and seedling biomass (dry weight) of lettuce decreased under BP (P < 0.05; Figs. 1 and 2). The root length of lettuce decreased, but the leaf length of lettuce increased under AS (P < 0.05; Figs. 1 and 2).

Figure 1
Seed germination indices of lettuce. Bars (means ± SE) with different letters mean statistically significant differences (P 0.05). The lowercase letters on top of the bars are presented as “a-c”, “a-d”, “b-d”, “g-i”, “d-f”, “f-h”, “e-g”, and “c-e” means “abc”, “abcd”, “bcd”, “ghi”, “def”, “fgh”, “efg”, and “cde”, respectively.
Figure 2
Seedling growth indices of lettuce. Bars (means ± SE) with different letters mean statistically significant differences (P 0.05). The lowercase letters on top of the bars are presented as “c-f”, “b-d”, “d-f”, “b-e”, “e-g”, “a-c”, “a-d”, “d-h”, “f-h”, and “c-e” means “cdef”, “bcd”, “def”, “bcde”, “efg”, “abc”, “abcd”, “defgh”, “fgh”, and “cde”, respectively.

Differences in the allelopathic intensity of the four asteraceae invasive plant species on lettuce seed germination and seedling growth

The germination potential of lettuce under BP was lower compared with that under AS (P < 0.05; Fig. 1). The germination index of lettuce noticeably declined in the following order: AS, EA, CC, and BP (P < 0.05; Fig. 1). The germination rate index of lettuce under BP was lower than that under the other three Asteraceae invasive plant species (P < 0.05; Fig. 1). The germination vigor index of lettuce under CC was lower than that under AS (P < 0.05; Fig. 1). The promptness index of lettuce under CC was lower than that under EA and AS (P < 0.05; Fig. 1). The germination vigor index and promptness index of lettuce under BP were also lower than those under EA and AS (P < 0.05; Fig. 1). The seedling height of lettuce under BP was lower than that under CC (P < 0.05; Fig. 2). The root length of lettuce under BP was lower than that under CC and EA (P < 0.05; Fig. 2). The green leaf area, leaf length, and root length of lettuce under CC were higher than those under the other three Asteraceae invasive plant species (P < 0.05; Fig. 2). The fresh weight of lettuce under CC was also higher than that under BP and AS (P < 0.05; Fig. 2).

Influence of silver nanoparticles with two particle sizes on lettuce seed germination and seedling growth

The germination rate index and seedling biomass (including fresh weight and dry weight) of lettuce decreased under AgNP20 and AgNP80 (P < 0.05; Figs. 1 and 2). The root length of lettuce also decreased under AgNP20 (P < 0.05; Fig. 2). The root length of lettuce under AgNP20 was lower than that under AgNP80 (P < 0.05; Fig. 2). The silver nanoparticles did produce any other significant effects on the lettuce SGe and SGr indices (P > 0.05; Figs. 1 and 2).

Influence of the allelopathic intensity of the four asteraceae invasive plant species on lettuce seed germination and seedling growth under two particle sizes of silver nanoparticles

The germination index, germination vigor index, promptness index, root length, and seedling biomass (dry weight) of lettuce decreased under the combined treatment of the four Asteraceae invasive plant species leaf extracts and silver nanoparticles regardless of particle size (P < 0.05; Figs. 1 and 2). The germination rate index of lettuce also decreased under the combined treatment of the four Asteraceae invasive plant species leaf extracts and silver nanoparticles regardless of particle size (except ASAgNP20) (P < 0.05; Fig. 1). The germination percentage and germination potential of lettuce decreased under CCAgNP20 and BPAgNP20 (P < 0.05; Fig. 1). The moisture content, fresh weight, and seedling height of lettuce decreased under BPAgNP20 (P < 0.05; Fig. 2). The leaf length, moisture content, and fresh weight of lettuce decreased under BPAgNP80 (P < 0.05; Fig. 2). Conversely, the leaf length and seedling height of lettuce increased under ASAgNP20 and ASAgNP80 (P < 0.05; Fig. 2). The moisture content of lettuce also increased under ASAgNP80 (P < 0.05; Fig. 2).

Influence of the allelopathic intensity of the four asteraceae invasive plant species on lettuce seed germination and seedling growth under two particle sizes of silver nanoparticles

The germination rate index, green leaf area, leaf length, root length, and fresh weight of lettuce under CCAgNP20 and CCAgNP80 were lower than those under CC (P < 0.05; Figs. 1 and 2). The green leaf area, leaf length, and seedling biomass (dry weight) of lettuce under EAAgNP20 were lower than those under EA (P < 0.05; Fig. 2). The germination rate index, green leaf area, leaf length, root length, and seedling biomass (includes fresh weight and dry weight) of lettuce under EAAgNP80 were lower than those under EA (P < 0.05; Figs. 1 and 2). The green leaf area, leaf length, moisture content, root length, and fresh weight of lettuce under BPAgNP20 and BPAgNP80 were lower than those under BP (P < 0.05; Fig. 2). Conversely, the germination index and promptness index of lettuce under BPAgNP80 were higher than those under BP (P < 0.05; Fig. 1). The root length of lettuce under ASAgNP20 and ASAgNP80 was also higher than that under AS (P < 0.05; Fig. 2).

DISCUSSION

Previous studies (Wang et al. 2018c, d, 2019d, 2020c, Carvalhoa et al. 2019CARVALHOA MSS, ANDRADE-VIEIRA LF, DOS SANTOS FE, CORREA FF, DAS GRAÇAS CARDOSO M VILELA LR. 2019. Allelopathic potential and phytochemical screening of ethanolic extracts from five species of Amaranthus spp. in the plant model Lactuca sativa. Sci Hortic 245: 90-98., Lyytinen & Lindström 2019LYYTINEN A LINDSTRÖM L. 2019. Responses of a native plant species from invaded and uninvaded areas to allelopathic effects of an invader. Ecol Evol 9: 6116-6123., Wei et al. 2020aWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020a. Heavy metal pollution improves allelopathic effects of Canada goldenrod on lettuce germination. Plant Biol 22: 832-838., b) indicated that the four Asteraceae invasive plant species, particularly C. canadensis, E. annuus, and B. pilosa, show signficant allelopathic interactions during the the germination of lettuce seeds, particularly on the germination power, germination rate and vitality, and response capability of seed germination of lettuce in this study. Thus, the seed germination of lettuce will decline noticeably under the allelopathic intensity produced by the four Asteraceae invasive plant species. This phenomenon could be caused by the allelochemicals generated, such as polyphenols, by the invasive plant species, which can have deleterious effects on nutrient absorption, carbon assimilation, and cell division (Djurdjević et al. 2012DJURDJEVIĆ L, GAJIĆ G, KOSTIĆ O, JARIĆ S, PAVLOVIĆ M, MITROVIĆ M PAVLOVIĆ P. 2012. Seasonal dynamics of allelopathically significant phenolic compounds in globally successful invader Conyza canadensis L. plants and associated sandy soil. Flora 207: 812-820., Fabbro et al. 2014FABBRO CD, GÜSEWELL S PRATI D. 2014. Allelopathic effects of three plant invaders on germination of native species: a field study. Biol Invasions 16: 1035-1042., Lyytinen & Lindström 2019LYYTINEN A LINDSTRÖM L. 2019. Responses of a native plant species from invaded and uninvaded areas to allelopathic effects of an invader. Ecol Evol 9: 6116-6123., Hsueh et al. 2020HSUEH MT, FAN CH CHANG WL. 2020. Allelopathic effects of Bidens pilosa L. var. radiata Sch. Bip. on the tuber sprouting and seedling growth of Cyperus rotundus L. Plants 9: 742.). These factors would have a strong impact on seed germination (Wang et al. 2018c, d, 2019d, 2020c, Carvalhoa et al. 2019CARVALHOA MSS, ANDRADE-VIEIRA LF, DOS SANTOS FE, CORREA FF, DAS GRAÇAS CARDOSO M VILELA LR. 2019. Allelopathic potential and phytochemical screening of ethanolic extracts from five species of Amaranthus spp. in the plant model Lactuca sativa. Sci Hortic 245: 90-98., Hsueh et al. 2020HSUEH MT, FAN CH CHANG WL. 2020. Allelopathic effects of Bidens pilosa L. var. radiata Sch. Bip. on the tuber sprouting and seedling growth of Cyperus rotundus L. Plants 9: 742., Wei et al. 2020aWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020a. Heavy metal pollution improves allelopathic effects of Canada goldenrod on lettuce germination. Plant Biol 22: 832-838., b, Krstin et al. 2021KRSTIN L, KATANI Z, PFEIFFER TŽ, MARONIĆ DŠ, MARINČIĆ D, MARTINOVIĆ A ČAMAGAJEVAC IŠ. 2021. Phytotoxic effect of invasive species Amorpha fruticosa L. on germination and the early growth of forage and agricultural crop plants. Ecol Res 36: 97-106.). Strangely, the four Asteraceae invasive plant species, particularly C. canadensis, E. annuus, and A. subulatus, can enhance the growth of lettuce seedlings, particularly on competitive sunlight capture and photosynthetic area. The cause could be the generation of reactive oxygen species (ROS) primarily generated within plant cells induced by the low concentration of allelochemicals released by the four Asteraceae invasive plant species, which may stimulate plant growth (Takao et al. 2011TAKAO LK, RIBEIRO JPN LIMA MIS. 2011. Allelopathic effects of Ipomoea cairica (L.) Sweet on crop weeds. Acta Bot Bras 25: 858-864., Zhang et al. 2012ZHANG SS, WANG B, ZHANG L, YU GD, TANG JJ CHEN X. 2012. Hormetic-like dose response relationships of allelochemicals of invasive S. canadensis L. Allelopathy J 29: 151-160., Wang et al. 2018c, d, 2019d, 2020c, Wei et al. 2020aWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020a. Heavy metal pollution improves allelopathic effects of Canada goldenrod on lettuce germination. Plant Biol 22: 832-838., b). This phenomenon has been identified as caused by hormones, as a response mechanism to environmental stress at low levels (Zhang et al. 2012ZHANG SS, WANG B, ZHANG L, YU GD, TANG JJ CHEN X. 2012. Hormetic-like dose response relationships of allelochemicals of invasive S. canadensis L. Allelopathy J 29: 151-160., Agathokleous et al. 2019AGATHOKLEOUS E, KITAO M, HARAYAMA H CALABRESE EJ. 2019. Temperature-induced hormesis in plants. J For Res 30: 13-20.). In addition, the nutrients in the allelochemicals of the four Asteraceae invasive plant species can promote seedling growth (Wei et al. 2020bWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020b. Combined allelopathy of Canada goldenrod and horseweed on the seed germination and seedling growth performance of lettuce. Landsc Ecol Eng 16: 299-306.). Thus, the four Asteraceae invasive plant species may decrease the seed germination but enhance the seedling growth of natives. The results suggest that the four Asteraceae invasive plant species can colonize new habitat via their allelopathic intensity on seed germination of natives first, but those competitors can obtain a higher fitness rate owing to their ability to more aggressively compete for resources compared with the natives. Based on this, it is necessary to eliminate invasive plant species as early as possible in the sowing of natives or in the early germination of natives to minimize the allelopathic effects of invasive plant species on the growth of natives.

Moreover, the allelopathic intensity of B. pilosa leaf extracts on lettuce seed germination was noticeably greater than that of the other three Asteraceae invasive plant species leaf extracts used in this study. However, it was unexpected that the A. subulatus leaf extracts had no apparent allelopathic intensity on lettuce seed germination in this study. Typically, the allelopathic intensity of the four Asteraceae invasive plant species on lettuce seed germination was markedly reduced in the following order: B. pilosa, C. canadensis, E. annuus, and A. subulatus. The main reason could be owing to the differences in the type and quantity of allelochemicals of the four Asteraceae invasive plant species. Thus, the allelopathic intensity on lettuce seed germination may perform a key role in the effective colonization of B. pilosa, C. canadensis, and E. annuus compared with A. subulatus. These results confirm the first hypothesis.

Silver nanoparticles normally decrease plant growth (Yin et al. 2012YIN LY, COLMAN BP, MCGILL BM, WRIGHT JP BERNHARDT ES. 2012. Effects of silver nanoparticle exposure on germination and early growth of eleven wetland plants. PLoS ONE 7: e47674., Wang et al. 2018c, 2020d, Wu et al. 2019bWU BD, ZHANG HS, JIANG K, ZHOU JW WANG CY. 2019a. Erigeron canadensis affects the taxonomic and functional diversity of plant communities in two climate zones in the North of China. Ecol Res 34: 535-547.). Similarly, silver nanoparticles were found to dramatically decrease the germination rate and vitality, competitive intensity for water and inorganic salts absorption, and growing competitive intensity of lettuce in this study. Thus, silver nanoparticles can inhibit plant growth. The main reason could be owing to the generated Ag ions that enter the environment from the silver nanoparticles (Guo et al. 2017GUO Z, CHEN GQ, ZENG GM, YAN M, HUANG ZZ, JIANG LH, PENG C, WANG JJ XIAO ZH. 2017. Are silver nanoparticles always toxic in the presence of environmental anions? Chemosphere 171: 318-323., Wang et al. 2018c, 2020d, Wu et al. 2019bWU BD, ZHANG HS, JIANG K, ZHOU JW WANG CY. 2019a. Erigeron canadensis affects the taxonomic and functional diversity of plant communities in two climate zones in the North of China. Ecol Res 34: 535-547.). In particular, Ag ions can be found in high concentrations in the root site of plant species (Vannini et al. 2014VANNINI C, DOMINGO G, ONELLI E, DE MATTIA F, BRUNI I, MARSONI M BRACALE M. 2014. Phytotoxic and genotoxic effects of silver nanoparticles exposure on germinating wheat seedlings. J Plant Physiol 171: 1142-1148.). It is believed these ions may decrease the chlorophyll contents and root elongation; inhibit cell division, the electron transport chain, and the synthesis of adenosine triphosphate synthesis; induce lipid membrane peroxidation; and disturb gene expression and the activity of metabolic enzymes (Holt & Bard 2005HOLT KB BARD AJ. 2005. Interaction of Silver (I) Ions with the respiratory chain of Escherichia coli: an electrochemical and scanning electrochemical microscopy study of the antimicrobial mechanism of micromolar Ag. Biochemistry 44: 13214-13223., Gubbins et al. 2011GUBBINS EJ, BATTY LC LEAD JR. 2011. Phytotoxicity of silver nanoparticles to Lemna minor L. Environ Pollut 159: 1551-1559., Benoit et al. 2013BENOIT R, WILKINSON KJ SAUVÉ S. 2013. Partitioning of silver and chemical speciation of free Ag in soils amended with nanoparticles. Chem Cent J 7: 75., Qian et al. 2013QIAN HF, PENG XF, HAN X, REN J, SUN LW FU ZW. 2013. Comparison of the toxicity of silver nanoparticles and silver ion on the growth of terrestrial plant model Arabidopsis thaliana. J Environ Sci 25: 1947-1956., Wu et al. 2019bWU BD, ZHANG HS, JIANG K, ZHOU JW WANG CY. 2019a. Erigeron canadensis affects the taxonomic and functional diversity of plant communities in two climate zones in the North of China. Ecol Res 34: 535-547.). In addition, silver nanoparticles that are 20 nm had a greater effect on the competitive intensity for water and inorganic salts absorption of lettuce than silver nanoparticles that are 80 nm. This difference is owing to the greater release of Ag ions from silver nanoparticles that have small particles (McGillicuddy et al. 2017MCGILLICUDDY E, MURRAY I, KAVANAGH S, MORRISON L, FOGARTY A, CORMICAN M, DOCKERY P, PRENDERGAST M, ROWAN N MORRIS D. 2017. Silver nanoparticles in the environment: Sources, detection and ecotoxicology. Sci Total Environ 575: 231-246., Wang et al. 2018c, 2020d, Wu et al. 2019bWU BD, ZHANG HS, JIANG K, ZHOU JW WANG CY. 2019a. Erigeron canadensis affects the taxonomic and functional diversity of plant communities in two climate zones in the North of China. Ecol Res 34: 535-547.). In addition, smaller silver nanoparticles can generate a higher level of reactive oxygen species, which can lead to toxicity toward plant growth (McGillicuddy et al. 2017MCGILLICUDDY E, MURRAY I, KAVANAGH S, MORRISON L, FOGARTY A, CORMICAN M, DOCKERY P, PRENDERGAST M, ROWAN N MORRIS D. 2017. Silver nanoparticles in the environment: Sources, detection and ecotoxicology. Sci Total Environ 575: 231-246., Wang et al. 2018c, 2020d, Wu et al. 2019bWU BD, ZHANG HS, JIANG K, ZHOU JW WANG CY. 2019a. Erigeron canadensis affects the taxonomic and functional diversity of plant communities in two climate zones in the North of China. Ecol Res 34: 535-547.). The results of this study apparently corroborate the second hypothesis.

In addition, based on previous results (Wang et al. 2018c), silver nanoparticles intensify the allelopathic effect of the four Asteraceae invasive plant species, particularly C. canadensis, E. annuus, and B. pilosa, on lettuce SGe and SGr, particularly on the competitive intensity for water and inorganic salts absorption, competitive intensity for sunlight capture, photosynthetic area, and growing competitive intensity in this study. Thus, silver nanoparticles noticeably increased the allelopathic intensity of invasive plant species on the SGe and SGr of natives, particularly on seedling growth. The finding may be explained by the following reasons: (I) invasive plant species and silver nanoparticles, particularly those with small particle sizes, pose an adverse effect on lettuce SGe and SGr in most cases. Thus, the combined treatment of these two factors generates a (negative) synergistic effect on lettuce SGe and SGr. (II) The combined treatment of these two factors would significantly attenuate the competitive intensity for water and inorganic salts absorption, competitive intensity for sunlight capture, and photosynthetic area of lettuce, and thus, noticeably decrease the growing competitive intensity of lettuce growth. (III) Phenolics, primarily polyphenols, are a group of the maximum abundant secondary compounds in plant species (i.e., allelochemicals for invasive plant species) (Zhang et al. 2011ZHANG SS, ZHU WJ, WANG B, TANG JJ CHEN X. 2011. Secondary metabolites from the invasive Solidago canadensis L. accumulation in soil and contribution to inhibition of soil pathogen Pythium ultimum. Appl Soil Ecol 48: 280-286., Djurdjević et al. 2012DJURDJEVIĆ L, GAJIĆ G, KOSTIĆ O, JARIĆ S, PAVLOVIĆ M, MITROVIĆ M PAVLOVIĆ P. 2012. Seasonal dynamics of allelopathically significant phenolic compounds in globally successful invader Conyza canadensis L. plants and associated sandy soil. Flora 207: 812-820., Wang et al. 2018d, 2020c, Marksa et al. 2020MARKSA M, ZYMONE K, IVANAUSKAS L, RADUŠIENĖ J, PUKALSKAS A RAUDONE L. 2020. Antioxidant profiles of leaves and inflorescences of native, invasive and hybrid Solidago species. Ind Crop Prod 145: 112123.), but the ecotoxicity of Ag ions released by silver nanoparticles (Guo et al. 2017GUO Z, CHEN GQ, ZENG GM, YAN M, HUANG ZZ, JIANG LH, PENG C, WANG JJ XIAO ZH. 2017. Are silver nanoparticles always toxic in the presence of environmental anions? Chemosphere 171: 318-323., Wang et al. 2018c, 2020d, Wu et al. 2019bWU BD, ZHANG HS, JIANG K, ZHOU JW WANG CY. 2019a. Erigeron canadensis affects the taxonomic and functional diversity of plant communities in two climate zones in the North of China. Ecol Res 34: 535-547.) on lettuce SGe and SGr may be increased by the weakly acidic phenolics, particularly polyphenols. Previous studies indicated that heavy metals are more toxic in acidic environments (Walker et al. 2004WALKER DJ, CLEMENTE R BERNAL MP. 2004. Contrasting effects of manure and compost on soil pH, heavy metal availability and growth of Chenopodium album L. in a soil contaminated by pyritic mine waste. Chemosphere 57: 215-224., Wang et al. 2018d, 2020c, Wei et al. 2020aWEI M, WANG S, WU BD, CHENG HY WANG CY. 2020a. Heavy metal pollution improves allelopathic effects of Canada goldenrod on lettuce germination. Plant Biol 22: 832-838.). Thus, these results may lend support to the third hypothesis. Consequently, silver nanoparticles, particularly those with small particle sizes, may facilitate the invasion process of the four Asteraceae invasive plant species. More importantly, most of the lettuce SGe and SGr indices under the combined treatment of B. pilosa and silver nanoparticles with two particle sizes were significantly lower than those under the combined treatment of the other three Asteraceae invasive plant species and two particle sizes of silver nanoparticles. Thus, the allelopathic effect of B. pilosa is significantly higher than that of the other three Asteraceae invasive plant species when subjected to pollution by silver nanoparticles. The main reason could be that the reactivity of the allelochemicals of B. pilosa is comparatively higher.

In summary, the four Asteraceae invasive plant species, particularly C. canadensis, E. annuus, and B. pilosa, generate apparent allelopathic intensity on the germination of lettuce seeds. Typically, the allelopathic intensity of the four Asteraceae invasive plant species on lettuce seed germination noticeably decreased in the following order: B. pilosa > C. canadensis > E. annuus > A. subulatus. In addition, silver nanoparticles increase the allelopathic intensity of the four Asteraceae invasive plant species, particularly C. canadensis, E. annuus, and B. pilosa, on lettuce SGe and SGr. Additionally, the allelopathic intensity of B. pilosa is significantly higher than that of the other three Asteraceae invasive plant species when subjected to pollution with silver nanoparticles. Therefore, increasing levels of silver nanoparticle pollution may stimulate the invasive behavior of the four Asteraceae invasive plant species, particularly B. pilosa, via their enhancement in the allelopathic intensity.

ACKNOWLEDGMENTS

This study was financed by Open Science Research Fund of Key Laboratory of Forest Plant Ecology, Ministry of Education (Northeast Forestry University), China (Grant No.: K2020B02), Key Research and Development Program of Changzhou, China (Grant No.: CJ20200013), and Jiangsu Collaborative Innovation Center of Technology and Material of Water Treatment. We are very grateful to the anonymous reviewers for the insightful and constructive comments that greatly improved this manuscript.

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Publication Dates

  • Publication in this collection
    13 June 2022
  • Date of issue
    2022

History

  • Received
    18 Oct 2020
  • Accepted
    3 Dec 2021
Academia Brasileira de Ciências Rua Anfilófio de Carvalho, 29, 3º andar, 20030-060 Rio de Janeiro RJ Brasil, Tel: +55 21 3907-8100 - Rio de Janeiro - RJ - Brazil
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