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Article

Azorean Vascular Plants with Potential Use in Constructed Wetlands with Horizontal Subsurface Flow

by
Vera B. Raposo
1,2,
Luís Silva
1,2 and
Sílvia Quadros
1,2,*
1
CIBIO—Research Centre in Biodiversity and Genetic Resources—InBIO Associate Laboratory, BIOPOLIS, University of the Azores, Campus of Ponta Delgada, Rua da Mãe de Deus, 9500-321 Ponta Delgada, Portugal
2
Faculty of Sciences and Technology, University of the Azores, Campus of Ponta Delgada, Rua da Mãe de Deus, 9500-321 Ponta Delgada, Portugal
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(22), 14681; https://doi.org/10.3390/su142214681
Submission received: 13 September 2022 / Revised: 26 October 2022 / Accepted: 28 October 2022 / Published: 8 November 2022
(This article belongs to the Special Issue Nature-Based Solutions and Biodiversity: Synergies and Implications)
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Abstract

:
Constructed wetlands are considered integrated ecosystems and a promising wastewater treatment option, relying on vegetation, soils, and microbial assemblages. The potential dispersal of effluents from domestic septic systems, the application of dairy farm effluents containing excessive nutrients and pathogens into pastures, and undertreated effluent discharge in coastal areas are some of the threats to water quality in the Azores. Constructed wetlands could be used in the Azores to protect and preserve the quality of drinking water sources and bathing waters. However, the most used plant species in other regions are considered as introduced in the Azores, where a considerable number of invasive plants and weeds are already present. Here, we present a review of the plant taxa already present in the Azorean flora with the potential to be used in constructed wetland systems, based on a literature review, and on the assessment of nine criteria. We evaluated 73 taxa, including mostly Cyperaceae, Poaceae and Juncaceae, showing that, although some of the top-ranking species were considered potentially noxious, several native and some naturalized taxa could be used for wastewater treatment. This work supports the implementation of constructed wetlands in the Azores, while minimizing the risk of new invasions.

1. Introduction

Since the 2000s, the term “nature-based solutions” (NBS) entered the scientific literature in the context of agricultural problems, land-use management, and water management [1]. NBS are defined by IUCN as “actions to protect, sustainably manage and restore natural or modified ecosystems, which address societal challenges (…) effectively and adaptively, while simultaneously providing human well-being and biodiversity benefits” [2]. The European Commission’s definition is broader and refers to NBS as those that not only use natural resources and processes but are also inspired and supported by natural ecosystems [2,3]. Within this context, here, we address the importance of constructed wetlands (CWs), in general, and in a perspective of their potential application in the Azores archipelago.

1.1. Constructed Wetlands as Nature-Based Solutions

CWs are wastewater treatment systems that use natural processes based on wetland vegetation (most commonly vascular plants), soils and their microbial assemblages [4,5]. There are many examples of CWs in temperate regions [6] that have been used for the treatment of different types of wastewaters, namely municipal, industrial, and agricultural [7,8,9,10].
CW classification depends on the macrophytes used—free-floating, floating leaves, emergent or submerged [7,8,10,11,12], and on the hydrology—free water surface or subsurface systems, the latter further classified as horizontal or vertical, according to their flow direction [5,13]. Several advantages of CWs include the requirement of low investment and maintenance costs, low energy consumption and the creation of habitats favourable to other species [12,14,15,16,17]. CWs present a favourable balance in the emission of greenhouse gases, compared to conventional wastewater systems [18], although this might depend on several factors, for example the selected plant species [19].
A horizontal subsurface flow (HSF) wetland is constructed as a bed filled with granular media of the appropriate size that is sealed by an impermeable layer and planted with vegetation. The wastewater enters and flows through the porous medium in a horizontal pathway up to the outlet zone. This medium acts as a filter, removing solids, organic compounds, nutrients, and biodegradable organic matter (measured through 5-day BOD), by microbial degradation, chemical, and physical processes. While the roots and rhizomes of the plants work as a substrate for attached bacteria, the whole plant is responsible for the uptake of nutrients, radial oxygen loss (oxygen diffusion from roots to the rhizosphere) and insulation of water preventing temperature variation [5,12,14]. Beyond the effects of water purification, plants fix carbon by photosynthesis. The main advantages of subsurface flow systems are the prevention of mosquitos and odours and the elimination of the risk of contact with the wastewater [4].
The choice of plants to use in CWs for phytoremediation depends on biomass, fast growth rate and tolerance to pollutant concentration [12,20]. Some of the most common macrophytes used in CWs are Phragmites australis (Cav.) Trin. ex Steud. and species belonging to the genus Typha [21].
Phragmites australis has been the preferred plant for application in CWs for wastewater treatment [22,23], due to its capacity to grow well under various types of habitats and climatic conditions. Its tolerance to different environments is explained by fast growth, high biomass accumulation, and high evapotranspiration rates, which protect the plants in case of toxic environments and flood conditions. In cold temperate maritime climates (e.g., Ireland), P. australis and Typha latifolia L. are predominant species in CWs [24]. Although P. australis is the most used macrophyte in Europe, it is not allowed in several regions, because it might invade natural wetlands [25,26,27,28]. Moreover, for instance, Canna indica has often shown better results than P. australis [12,19]. Therefore, other species must be tested for CWs.

1.2. Case Study Azores

1.2.1. Domestic effluents

In the Azores archipelago, the main method for domestic wastewater treatment is the use of decentralized systems with septic tanks (ST), serving 78% of the population, and in some islands being the unique treatment available [29]. However, when installed in suboptimal conditions (e.g., high effluent loads, inadequate soil type and drainage, proximity to sensitive aquatic ecosystems such as coastal areas or wetlands and shallow aquifers), ST can have a high potential for water pollution [30,31,32]. The absence of proper treatment can result in nearby groundwater and surface waters contamination, potentially affecting human health and environmental quality due to high concentrations of nitrates, and the presence of faecal microorganisms, leading to disease outbreaks, antibiotic resistance in aquatic microorganisms, or eutrophication of surface waters which cause loss of biodiversity and a decline in the aquatic ecosystem services [31,32].

1.2.2. Agricultural effluents

Artificial pastureland dominates the land cover in the Azores, where 51.9% (120,632 ha) of the land is utilized for agriculture, of which 74.6% corresponds to pasture. Recently, the area occupied by seasonal forage maize has also increased, corresponding to 22.1% of the utilized agricultural area. The number of cattle ascended to 282,820 animals in 2019, of which 95,385 were dairy cows [33]. Those pastures correspond to grazing systems where cattle can circulate following a utilization scheme defined by the farmers [34]. In the past, the production was extensive; thus, there was no need for animal housing, and the effluent production was lower. The excessive application of synthetic fertilizers rich in nitrogen (N) and phosphorus (P) associated with accentuated orography and high levels of precipitation favours the runoff of nutrients and pollution of water bodies [35,36]. In order to protect the watersheds and control the eutrophication, the regional government acquired about 300 ha of pasture lands to forest with endemic species [37]. However, in recent years, the intensification of production in the bigger islands has led to an increase in the extension and frequency of mowing, increased animal housing and, consequently, more effluent accumulation. This effluent is stored and spread in the soil as fertilizer without any treatment, at least twice per year. The application of synthetic and organic fertilizers and animal waste leaching have resulted in high concentrations of nitrate in groundwater, and consequently, in non-compliance with European Union and national water quality regulations [38].

1.2.3. Potential of CWs in the Azores

The CW technology could be applied to treat domestic and dairy effluents in the Azores, since it is a viable, cost-effective, and efficient alternative for small and decentralized agglomerates [39]. In warmer climates and insular territories, such as Mayotte (French outermost territories) and the Canary Islands, CWs showed good results in wastewater treatment. In Mayotte tropical weather, CWs planted with Thysanolaena maxima and Typha angustifolia showed reduced rates of COD, suspended solids and total Kjeldahl nitrogen that satisfied French national quality objectives for domestic wastewater treatment [40].
In agglomerations with more than 2000 population equivalents, urban wastewater should be collected and treated in centralized systems, before discharge (Council Directive 91/271/EEC). If the discharges occur in sensitive areas (i.e., freshwater lakes, estuaries, coastal waters, and surface freshwaters for human consumption), a more exigent quality of discharge is required, regarding microbiological and nutritional parameters. In those cases, CWs could contribute to improving the overall physical–chemical and microbiological quality of secondary effluents, reducing the impact of their discharge in water bodies [41].
Within this framework, this paper presents a review of the plant taxa already present in the Azorean Flora with the capacity to be used in CW systems, allowing for the implementation of those wastewater treatment systems in the Azores, without risking the loss of biodiversity through the importation of new invasive species.

2. Materials and Methods

2.1. Climate and Geographical Framework

The Azores archipelago, located in the Central North Atlantic Ocean (37–40° N, 25–31° W), 1400 km from Portugal mainland, is one of the five archipelagos included in the Macaronesia geographical region. It is composed by nine oceanic volcanic islands scattered along more than 600 km, with a total land surface of 2325 km2. The archipelago is divided into three groups (Figure 1): Flores and Corvo (western group), Terceira, Graciosa, Pico, São Jorge and Faial (central group), and São Miguel and Santa Maria (eastern group).
The Azores climate is influenced by its location in the middle of the Atlantic Ocean, where there are low-pressure zones alternating with the presence of a large high-pressure system, the Azores anticyclone, and by the orography of the islands [42]. The Azores temperate oceanic climate, also designated temperate maritime climate, is characterized by mild temperatures, low thermal amplitudes, and precipitation well distributed during the year. According to the last census [33], in the Azores, there are 236,657 inhabitants, and the average population density was 101.8 people per km2. In the Azores archipelago, 52% of the population lives in agglomerates with less than 2000 inhabitants, contrasting with 42% in the mainland territory [43].

2.2. Flora of the Azores

About 6112 terrestrial species (6164 taxa) are given for the Azores, of which 411 are endemic. The vascular plants (Pteridophyta and Spermatophyta) include a total of about 1000 taxa [44]. However, recent reports indicate that the entire vascular flora, also including cultivated plants, includes more than 5000 taxa.
The Azorean plant cover before human settlement was most likely dominated by different vegetation belts corresponding to different types of scrubland, woodland and forest [45]. However, changes in land use have led to a drastic reduction in natural forest cover and the expansion of exotic woodland and production forest [45,46]. Besides land cover change, invasive species, including a large number of plant taxa that are recognized as problematic invaders worldwide, constitute a major threat to the preservation of the remaining natural plant communities in the Azores [47,48].

2.3. Evaluation of the Azorean Vascular Flora for CW Projects

In the study carried out by [23], the species used throughout the world in wetlands built with the horizontal subsurface flow were listed. The respective genera, in total 21, were listed, and their existence in the Azores archipelago was verified according to [44], the Azorean Biodiversity Portal and more recent reports. In addition, the genus Lolium has been added because it is known to tolerate large amounts of organic matter.
From the resulting list of genera, all taxa belonging to each genus and cited for the Azores were listed (73 taxa), according to the above references. In the case of Lolium arundinaceum (Schreb.) Darbysh. (Festuca arundinacea Schreb.), since the circumscription of the group is not clear [49], we included the species belonging to both genera. No data were available to distinguish between subspecies in terms of their potential use in CWs; therefore, our analysis relied on the available data at the species level.
This selection resulted in a list of existing species in the region with the potential to treat wastewater in CWs with the horizontal subsurface flow. Each species was described as to its (1) life form, (2) habitat, (3) status in the region, (4) aboveground biomass, (5) storage organs, (6) potential growth rate, (7) type of reproduction, (8) cultivation, and (9) tolerance to nutrient loadings and removal efficiency. To obtain a ranking of the most useful species, each criterion was classified between 0 and 4 points, according to species traits (Table 1).
Moreover, all species were classified according to their possible noxious status—invasive species or weeds. Regarding the origin of the species, we attributed a score of 0 points to endemic taxa since they usually correspond to relatively rare plants, circumscribed to habitats, to a sub-archipelago or an island e.g., [50]. Moreover, we wanted to avoid interfering with the evolutionary processes taking place in their natural populations e.g., [51]. In addition, in general, those taxa did not show relevant traits to be used in wastewater treatment.
Finally, we also considered if the species were presently used in cultivation in the Azores, attributing a positive score, from 2 (limited cultivation) to 4 (extensive cultivation), to that situation.
Information regarding plant traits used to score the evaluated taxa was obtained from the following sources: [52,53,54,55,56,57,58,59,60,61].
The resulting list of taxa was ranked according to the percentage value obtained by dividing the obtained score by the maximum total score possible (i.e., 4 × 9 = 36 points). The species were ordered into quartiles: 1st quartile—score < 25%; 2nd quartile—25 ≤ score < 50; 3rd quartile—50 ≤ score < 75; 4th quartile—score ≥ 75.
We applied a Mann–Whitney nonparametric test to compare the total scores from noxious and non-noxious plant species. Additionally, we applied a CATPCA—principal components analysis for categorical data to the item score dataset, to determine what were the most discriminating items and to assess possible differences among noxious and non-noxious plant species. The statistical analyses were performed using IBM SPSS version 26.

3. Results and Discussion

The resulting list integrates a total of 73 species distributed in 9 families and 21 genera (Supplementary Table S1). The Cyperaceae and the Poaceae dominated, followed by the Juncaceae (Figure 2). In the same direction, the genus Carex included more species (20), followed by Juncus (10), and Cyperus (8) (Supplementary Table S1).
After scoring all 73 taxa according to the 9 criteria, the families including more taxa in the third and fourth quartiles (Figure 3) corresponded to the Cyperaceae (one in the 4th, seven in the 3rd) and Poaceae (one in the 4th, six in the 3rd), Typhaceae and Araceae (one taxa in the 4th), Juncaceae (three in the 3rd), and Cannaceae and Lamiaceae (one in the 3rd). The taxa included in the 4th quartile included Colocasia esculenta, Bolboschoenus maritimus, Arundo donax and Typha domingensis.
Only slight differences in some of the items were found among the four taxa in the 4th quartile (Figure 4). We scored T. domingensis a little lower than the others, regarding reproduction and cultivation. B. maritimus scored more in the category of origin since it was, among those taxa, the only one considered to be native to the Azores. The taxa in the 3rd quartile appeared to be divided into four groups within each taxa sharing the same score, but with slight differences, for the different item scores within those groups.
Figure 5 shows a summary of the score distribution for the global set of taxa, for the taxa at the bottom two quartiles, and for those taxa at the top two quartiles.
Regarding life forms (Figure 5a), we found a pronounced increase in taxa with a more adequate life strategy at the two top quartiles and a very similar situation regarding the type of habitat of those taxa (Figure 5b). Regarding origin (Figure 5c), we found no endemic species at the top two quartiles and a predominance of naturalized taxa, although with a considerable contribution of native taxa (about one-third). Considering the aboveground biomass (Figure 5d), there was a clear distinction between top-rank and bottom-rank species, with the former including mostly medium potential, but also including about one-fifth with high potential in this topic. A similar situation was found for belowground biomass (Figure 5e), although almost 50% of the top-ranked taxa classified with a high potential due to the presence of storage organs. The growth rate (Figure 5f) did not show a clearly different pattern for the different groups of taxa. However, regarding the type of reproduction (Figure 5g), namely those taxa clearly including effective vegetative propagation, the proportion of taxa with this ability was clearly higher in the top-ranking taxa. The proportion of cultivated taxa (Figure 5h) was, in general, low. Finally, regarding tolerance to water contaminants (Figure 5i), for most of the top-ranking taxa, references were found documenting this capability.
Meanwhile, in the global species dataset, about one-third of the taxa were found to be potentially noxious (i.e., weeds or invaders), and this proportion raised to above 50% when considering the top-ranking species only (Figure 6).
Due to the similar characteristics of reproduction, development and morphology, the discussion is reviewed by family.
There was a significant difference between the total scores of noxious and non-noxious plant species, with the former obtaining larger scores (Figure 7; see Supplementary Materials).
The CATPCA originated two dimensions explaining more than 90% of the variance in the item score matrix (Figure 8). The first dimension was more related with growth rate, belowground biomass and the category of origin, while the second was more related with habitat type, category of life-form, and category of origin (Supplementary Materials). The noxious species tended to show larger values on the first dimension; however, the native Bolboschoenus maritimus showed relatively high values in the two dimensions.
Cyperaceae
Given the genera selected according to the literature, it was expected that this family would have the largest contribution, given its importance in the Azores and the worldwide [60].
From the eight species of Cyperus, four were included in the top 10 and five in the 3rd quartile, with three being considered as potentially noxious. Plants from the genus Cyperus are commonly used in CWs [62,63], and they play an important role in the maintenance and improvement of water quality [64]. Some studies showed a removal of up to 92% of total nitrogen and significant metal sequestration [65,66]. Ref. [67] verified that C. longus (17th in our study) can be a biological wastewater purifier through the removal of heavy metals. Cyperus eragrostis (27th in our study) was used in CWs in Australia as part of tertiary treatment [68,69,70], but the authors considered that more studies would be needed to test the efficiency of these plants. This taxon has recently been considered invasive in the Azores and in wetlands, although its expansion is somewhat limited, usually to scattered individuals or small groups of plants. Several studies using C. involucratus (6th in our study) showed that this species could be useful to treat wastewaters due to its fast growth, adaptation to different environments and nutrient removal [71]. Ref. [72] tested several species in a CW to treat seafood wastewater and concluded that C. involucratus showed high N and BOD5 uptake and high biomass production. Ref. [73] verified that this species removed 99% of NH4-N and 64% of inorganic N, concluding that it could be a good option to be used in CWs for N removal. Cyperus alternifolius (8th in our study) has also been studied in CWs to treat wastewater. This species showed good results for P removal in different wastewaters [74,75,76]. A study conducted by [77] comparing C. alternifolius with Vetiveria zizanioides to treat piggery wastewater revealed that the removal of N, P and some heavy metals by C. alternifolius was 4–7 times higher.
Bolboschoenus maritimus (2nd in our study) is a native plant from the Terceira and Faial islands, and it is adaptable to wetland habitats. It is propagated by rhizomes and has a reasonable amount of aboveground biomass. Associated with that, the fast growth and good tolerance to high nutrient loadings make this species the best option in the Azores to treat effluents in CWs with HSSF, according to this methodology. This is not one of the most common species used in CWs; however, some studies showed its efficiency in nutrient accumulation [78]. In the Azores, this species was already tested to treat domestic effluents and showed good performance in phosphorus, organic matter and faecal coliforms removal, and a growth rate comparable to that of A. donax [41].
While Eleocharis sphacelata is the most common species of the genus to be used in CWs with HSSF, E. palustris (11th in our study) and E. multicaulis (18th in our study), both in the 3rd quartile, are native species from the Azores, which we considered to accumulate only medium levels of biomass above and belowground. The elemental percentages of C, N and P for the aboveground biomass of E. palustris in CWs was determined by [79], and the results showed a high N percentage when compared to other species such as Carex nebrascensis, Juncus balticus, Scheonoplectus maritimus (=Bolboschoenus maritimus), S. acutus, S. pungens, and T. latifolia. Meanwhile, E. multicaulis is characteristic of oligotrophic environments, i.e., with low nutrient levels.
Typhaceae
Typha domingensis (4th in our study) is the only species belonging to the genus Typha recorded in the Azores, but its distribution is restricted to Santa Maria Island, although probably being cultivated on other islands in artificial wetlands. Notwithstanding the well-known phytoremediation effect and nutrient removal of T. latifolia, T. domingensis has also had promising results in several studies [80,81,82]. T. domingensis presents the morphological characteristics to be used in CWs, and the previous studies conducted with this species raise it to the 4th position of the ranking. However, it has recently been considered as invasive in the Azores, in water streams, where it occurs out of cultivation, although with a limited extension.
Araceae
Colocasia esculenta (3rd in our study) is an abundant species in all the Azores archipelago that is easy to obtain and maintain in cultivation. Despite being a potentially invasive species in many places, in the Azores and Madeira Island [48], particularly along water streams and in steep, wet coastal areas, it has been widely used for commercial and agricultural purposes in the Azores, being planted but also frequently escaping from cultivation, forming from small groups of plants to dense stands, resulting from vegetative propagation of the rhizomes. Previous research showed removal of nitrate, phosphate and organic matter, and tolerance to very high COD concentrations. There are studies with C. esculenta in domestic wastewater treatment with promising results for nutrient and heavy metal removal [83,84,85,86,87,88,89]. In Tanzania, results of this species used in CWs showed that phosphorus, sulphate, ammonia, and COD can be effectively removed [90]. Moreover, C. esculenta was revealed to be a technically and economically viable option for CWs to treat rice mill wastewater [83].
Juncaceae
In the Azores, we have records of ten species of Juncus. According to our results, three species were in the 3rd quartile, and the remaining were distributed among the 2nd and 1st quartiles. Juncus maritimus, J. acutus and J. effusus are all common in the Azores, the first two mostly near the coast, and the latter at inland wetlands (e.g., lake and water stream margins, wet pastureland). Plants belonging to this genus are considered helophytes and are tolerant to water-clogged soils and, in some cases, are halotolerant.
Juncus effusus has been used in the United States of America [23,91] in domestic wastewater treatment with positive results for total phosphorus, total Kjeldahl nitrogen and ammoniacal nitrogen removal. It has been also used in CWs in several regions in mainland Portugal [92,93,94]. The occurrence of this species near pastures where the rainwater flows with high concentrations of nutrients due to leaching shows the probable good adaptation to agricultural wastewaters, particularly from cattle farms.
Juncus acutus has been used in CWs in several studies. This species tolerates drought, flood, and salty conditions [95] and can be used in different environments. Ref. [20] demonstrated that J. acutus is appropriate for phytoremediation purposes, especially in antibiotic and contaminant removal. J. bofonius is also a native species from the Azores; however, the biomass of this plant is very low, which according to some studies, can affect removal efficiency.
Cannaceae
Canna indica is found in the Azores both as an ornamental plant in gardens, but it also frequently escapes from cultivation along the margins of exotic woodland, agricultural land, and water streams, ranking 5th in our analysis, being the first species in the 3rd quartile. It is one of the main emergent and ornamental macrophytes in CWs in the Mediterranean countries [63], being used for various purposes such as domestic, municipal, and agricultural wastewater treatment [62,96]. Ref. [97] used this species to treat dairy-farm effluents with high concentrations of organic matter and obtained very high COD removal. Beyond the improvement of water quality, C. indica also contributes to the aesthetic value of the locations.
In some cases, fibrous-root plants, as in the case of C. indica, Juncus, and C. esculenta, displayed higher photosynthesis and nutrient removal when compared to thick-root plants [98]. The rhizosphere of wetland plants is the most important element of the CW, where the physicochemical and biological processes take place and all components (i.e., plant tissues, wastewater, microorganisms, substrate) contact directly [70,99,100]. Furthermore, some studies indicated a relation between nutrient removal and plant root number and root surface area [101,102].
Lamiaceae
Mentha spicata is cultivated in the Azores at very small stands as an aromatic herb, being occasionally found as escaping cultivation, ranking 13th in our analysis. Ref. [103] tested M. spicata in CWs together with other species and obtained high removals for BOD5, TSS and faecal coliforms. This species showed a good response to high levels of P and N [104]. Ref. [105] used M. spicata to treat effluents of aquaponics, and the removal of NH4 and PO4 was 48% and 55%, respectively.
Poaceae
According to the genera cited in the literature as of interest in CWs, we listed 24 taxa, most of which (17) ranked in the bottom two quartiles. Of the remaining 7 taxa, Arundo donax ranked 1st, Stenotaphrum secundatum 7th, two Phalaris species ranked 15th and 16th, two Glyceria species ranked 19th and 20th, and Panicum repens as 22nd. The family is one of the most represented in the Azores, since it includes numerous weeds, forage and lawn species. However, the plants belonging to Poaceae are not commonly used in wastewater treatment due to the low biomass of aerial organs. Nonetheless, several are used in pastureland (e.g., Lolium spp.), being able to tolerate high amounts of organic matter (e.g., manure applications).
Arundo donax was introduced intentionally in the Azores to hedgerows, to control soil erosion, handcraft, ornamental, and agriculture, but when established, it caused drastic ecological changes and affected several endemic and native species, including vascular plants and seabirds [48,106]. It has invaded large areas in all the archipelago, particularly along water streams and in coastal areas, including very steep sea cliffs. Presently, it is classified as one of the 100 invasive species in Macaronesia [48]. Despite that A. donax is attracting attention to be used in CWs due to these promising results [107,108,109,110], encouraging further cultivation and dispersal would be a threat to native and endemic plants and to coastal habitats.
Stenotaphrum secundatum has been extensively used in the Azores in lawns, but it tends to escape cultivation and expand into the surrounding natural areas, including coastal and inland ecosystems, completely changing the vegetation structure [48]. Some studies demonstrated the capacity of S. secundatum to remove nutrients from different types of wastewater [62,111,112].
Phalaris arundinacea has been used in CWs in consortium with other plants in the Czech Republic and the United States [23,113]. This species can survive in poorly drained regions and can withstand long periods of flooding [114].
Most of the existing studies in CWs using Glyceria are focused on Glyceria maxima; however, this species is not recorded for the Azores. Some studies demonstrated the potential of G. declinata and G. fluitans (19th and 20th in our study) for phytoremediation, especially in heavy metal reduction and nutrient uptake [115,116], although the above biomass is very low. Sorghum halapense was studied by [117] and presents the morphological requirements to be used in CWs; however, this species is a worldwide weed, which could deter its more extensive use.
Panicum repens is a very common plant in wetland areas and is very difficult to control [118]. Some studies demonstrated that P. repens is suitable to reduce metals [119,120] and that it can also reduce water salinity [121].
Other families
The Onagraceae were represented in our list by three species of Epilobium, although all scored relatively low (28th to 30th), corresponding to small stature hemicryptophytes mainly adapted to terrestrial environments. In addition, they present low biomass, and no wastewater treatment studies were found for these taxa. Epilobium obscurum can survive in mesotrophic habitats [58]; however, no data about nutrient removal were found with this species. Regarding Rosaceae, the selected genus according to the literature corresponded to Filipendula vulgaris, ranking 31st in our analysis, typical of terrestrial habitats, with low biomass and for which no studies on nutrient removal were found. For both families, studies were performed with other species of the same genera (E. hirsutum and F. ulmaria) by [113] in the Czech Republic.
The experimental tests to be carried out with the results of this study should consider mixed cultures, with two or more species, since according to several authors [23,103,122,123], the association of species represents higher efficiencies of pollutant removal. Since some species only occur on specific islands of the Azores (e.g., B. maritimus on Terceira and Faial islands and T. dominguenses on Santa Maria island), when selecting species to be used, preference should be given to the best ranked species occurring locally.

4. Conclusions

Several of the most common plant taxa used in CWs with HSF are classified as invasive species in the Azores; a proposal of alternatives is of utmost importance. Given its potential as a top invasive species, we do not recommend the use of Arundo donax in CWs in the Azores, although it ranked first in our analysis. Furthermore, Bolboschoenus maritimus and the three species of Juncus with the highest scores all are considered native in the Azores, and their use in CWs in the region should be further encouraged if the material used comes from the Azores and no threat to the natural populations of these species is ensured. A similar approach would be acceptable for the Eleocharis species. Regarding Typha domingensis and Canna indica, their use in CWs in the Azores should be considered in those cases where escape from cultivation could be avoided, which might be problematic in terms of logistics. Nonetheless, both species are presently being used as ornamental plants in gardens and artificial lakes. More research would be needed to better understand their present and potential impact on natural habitats. Finally, Colocasia esculenta is presently being used extensively in the Azores as an agricultural crop, particularly along water stream margins; therefore, its use in CWs could be envisioned if regulations and procedures would be defined and implemented to avoid further expansion into natural environments.
As a whole, this study showed that in the Azores, plant resources are available to ensure the development of further research and pilot studies devoted to the use of CWs in water treatment approaches.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su142214681/s1, Table S1: Numerical assessment of criteria for each species. LIF: life form; HAB: habitat; CAT: category of origin; ABO: aboveground biomass; BEL: belowground organs; GRO: potential growth rate (in a season); REP: reproduction; CUL: cultivation; TOL: tolerance to nutrient loadings and removal efficiency: NOX: noxious (weed or invasive). The total value was calculated by dividing the obtained score by the maximum total score possible; File S1: Statistical analyses.

Author Contributions

Conceptualization, V.B.R. and S.Q.; methodology, V.B.R., L.S. and S.Q.; validation, L.S.; writing—original draft preparation, V.B.R.; writing—review and editing, V.B.R., L.S. and S.Q.; supervision, S.Q.; funding acquisition, S.Q. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by MITIMAC “Mitigacion del cambio climático através de la innovatión em el ciclo del agua mediante tecnologias bajas en carbono” (MAC2/1.1a/263), co-financed by the Interreg (MAC 2014–2020) Cooperation Program, by DRCTD (Direção Regional da Ciência e Transição Digital), and by FEDER funds through the Operational Programme for Competitiveness Factors.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 1. Location of the Azores archipelago in the Northeast Atlantic.
Figure 1. Location of the Azores archipelago in the Northeast Atlantic.
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Figure 2. Distribution of evaluated taxa by families.
Figure 2. Distribution of evaluated taxa by families.
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Figure 3. Number of taxa that were evaluated by plant family, discriminating their respective quartile, was determined based on their total score calculated as a percentage of the possible maximum score per species.
Figure 3. Number of taxa that were evaluated by plant family, discriminating their respective quartile, was determined based on their total score calculated as a percentage of the possible maximum score per species.
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Figure 4. Scores of the evaluated taxa with higher ranks (third and fourth quartiles) for each of the nine criteria (different colours): LIF—life form, Hab—habitat, CAT—category of origin, ABO—aboveground biomass, BEL—belowground biomass, GRO—growth rate, REP—reproduction, CUL—cultivation, TOL—tolerance. For the complete table, see Supplementary Table S1. Here, the scores are presented as raw (i.e., 0, 2 or 4) and not as a percentage.
Figure 4. Scores of the evaluated taxa with higher ranks (third and fourth quartiles) for each of the nine criteria (different colours): LIF—life form, Hab—habitat, CAT—category of origin, ABO—aboveground biomass, BEL—belowground biomass, GRO—growth rate, REP—reproduction, CUL—cultivation, TOL—tolerance. For the complete table, see Supplementary Table S1. Here, the scores are presented as raw (i.e., 0, 2 or 4) and not as a percentage.
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Figure 5. Score distribution (0, 2, or 4) for life form (a), habitat (b), category of origin (c), aboveground biomass (d), belowground biomass (e), growth rate (f), reproduction (g), cultivation (h) and tolerance to a high concentration of nutrients (i), for the global set of taxa and for the taxa located at the bottom or top two quartiles.
Figure 5. Score distribution (0, 2, or 4) for life form (a), habitat (b), category of origin (c), aboveground biomass (d), belowground biomass (e), growth rate (f), reproduction (g), cultivation (h) and tolerance to a high concentration of nutrients (i), for the global set of taxa and for the taxa located at the bottom or top two quartiles.
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Figure 6. Percentage of taxa considered as noxious (i.e., weeds or invasive plants) in the global dataset, in the taxa located at the two lowest quartiles and in the top-ranking taxa (two upper quartiles).
Figure 6. Percentage of taxa considered as noxious (i.e., weeds or invasive plants) in the global dataset, in the taxa located at the two lowest quartiles and in the top-ranking taxa (two upper quartiles).
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Figure 7. Comparison of the total scores from noxious (1) and non-noxious (0) plant species. Boxplot including frequency distribution of total score for both groups.
Figure 7. Comparison of the total scores from noxious (1) and non-noxious (0) plant species. Boxplot including frequency distribution of total score for both groups.
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Figure 8. Results of the CATPCA − principal components analysis for categorical data. Plot with species scores for both extracted factors (dimensions 1 and 2).
Figure 8. Results of the CATPCA − principal components analysis for categorical data. Plot with species scores for both extracted factors (dimensions 1 and 2).
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Table
Table 1. Description and quantification of the criteria.
Table 1. Description and quantification of the criteria.
CriteriaParametersPoints
1Life formHelophyte, Hydrophyte, Hygrophyte4
Proto-hemicryptophyte, Hemicryptophyte, Microphanerophyte2
Therophyte0
2HabitatWetlands4
Terrestrial or wetlands, Terrestrial or Humid soils2
Terrestrial0
3Category of originNative4
Naturalized, Casual2
Endemic0
4Aboveground biomassLarge aboveground organs (>1.5 m height, large leaves with >0.5 m long)4
Medium sized aboveground organs (<1.5 m height, leaves up to 0.6 m long)2
Thin, slender stems or culms and small leaves (< 1 m height, leaves up to 0.5 m and 0.1 m wide)0
5Belowground organsLarge rhizome, Corm4
Rhizome, tuberose root, bulb, tuber2
Short fibrous roots0
6Potential growth rate (In a season)High4
Medium2
Low0
7ReproductionVegetative reproduction4
Mainly by seed but some vegetative spread2
Only by seed0
8CultivationCultivated in large areas4
Cultivated in small areas2
Not cultivated0
9Tolerance to nutrient loadings and removal efficiencyHigh tolerance and/or high nutrient removal4
Presence in habitats with nutrients, but no data on nutrient removal2
No tolerance or no data0
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Raposo, V.B.; Silva, L.; Quadros, S. Azorean Vascular Plants with Potential Use in Constructed Wetlands with Horizontal Subsurface Flow. Sustainability 2022, 14, 14681. https://doi.org/10.3390/su142214681

AMA Style

Raposo VB, Silva L, Quadros S. Azorean Vascular Plants with Potential Use in Constructed Wetlands with Horizontal Subsurface Flow. Sustainability. 2022; 14(22):14681. https://doi.org/10.3390/su142214681

Chicago/Turabian Style

Raposo, Vera B., Luís Silva, and Sílvia Quadros. 2022. "Azorean Vascular Plants with Potential Use in Constructed Wetlands with Horizontal Subsurface Flow" Sustainability 14, no. 22: 14681. https://doi.org/10.3390/su142214681

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