Evaluation of High Andean Plant Species in the Absorption and Translocation of Heavy Metals in the Moorlands of Reten IchuBamba, Ecuador

Abstract

Phytoremediation is based on the use of plants to decontaminate water and soil. In this work, the capacity of high Andean vegetation in the absorption and translocation of heavy metals was analyzed. Species were identified to analyze the presence of metals in roots, stems, and leaves by spectrometry. The translocation factor was determined and analyzed by means of pattern clusters. Based on the floristic inventory, the dominance of the Poaceae and Asteraceae families was determined, and 12 plant species with a high importance value were selected. According to the ICP-AES, mercury (951.07 mg/kg) was determined in the roots of Lachemilla orbiculata, and chromium (21.88 mg/kg) in Carex bonplandii. Arsenic (2.79 mg/kg) was detected as being significantly higher than the values recorded in lowland plants. Cadmium mobility was high in all species, reaching higher values in Baccharis salicifolia (86.28%) and Calamagrostis intermedia (37.16%). Rumex acetocella accumulated lead in leaves (9.27%), while Taraxacum officinale (1.20%) and Calamagrostis intermedia (1.20%) accumulated silicon. Stabilization of chromium, mercury, and sodium was determined in the roots without translocation to higher organs. Finally, cluster analysis showed physiological interactions between metals as a toxicity mitigation mechanism affecting mobility. These findings suggest that they are hyperaccumulator species.

1. Introduction

Climate change has become a global threat, harming the population and the environment, as a consequence of the development of industrial activities, inefficient food security, droughts, floods, which are mainly caused by mining, waste burning, and wastewater discharge [1,2,3]. Thus, during the last 50 years, there has been an accelerated expansion of industrialization, leading to the exploitation of natural resources and thus aggravating the problem of environmental pollution [4].

In Ecuador, there is evidence of microbial contamination and the presence of heavy metals such as arsenic, cadmium, copper, mercury, and lead in water sources, which has caused serious health risks [1,5,6,7]. Thus, it is presumed that in the province of Chimborazo, there could be a great deal of heavy metal contamination. Several studies have determined that arsenic contamination exceeds the permissible limit defined by the World Health Organization (WHO) of 10 ppb in 107 countries, affecting approximately 230 million people worldwide [8].

The Andean paramos are ecosystems of great biological diversity and altitude located above 3000 m above sea level, with a cold climate and annual rainfall between 700 and 3000 mm. This region provides ecosystem services and represents 86% of endemic angiosperm plant species. However, its composition has been altered due to anthropogenic activities and climate change [9,10,11,12]. Several studies indicate that the presence of metal contamination in rivers is due to small-scale gold mining activities [6,13]. The research carried out points to the urgent need for environmental and public health intervention to counteract contamination by metals in the moorlands of Ecuador.

Phytoremediation is an emerging technology based on the use of plants that use natural mechanisms such as phytoextraction, phytostabilization, phytotovolatilization, and phytodegradation to degrade, accumulate, and eliminate pollutants, making it a cost-effective and sustainable alternative for the remediation of contaminated soils and waters [14,15,16,17,18]. In addition, several research studies have demonstrated the efficiency of plants in the degradation of pollutants such as hydrocarbons [19]. Thus, for the decontamination of domestic wastewater, aquatic plants such as Canna, Hyacinth, and Typha have been used to improve water quality [20].

For at least half a century, the tolerance of plants to heavy metals, which in some cases occurs naturally as mineral components of the soil, has been recorded [21]. It is worth mentioning that there are around 400 known species of metal-accumulating plants worldwide, where the Brassicaceae family stands out, as it has several species that can accumulate more than one metal [22]. Generally, native species with fast growth, abundant biomass, and easy adaptation have a high potential for phytoremediation [23].

In this context, the objective of this study was to evaluate the absorption and translocation of heavy metals by high Andean plant species of the Reten Ichubamba paramo. It was proposed that certain species could play a key role in the remediation of contaminated soils and water sources through their ability to accumulate or transport heavy metals, which would mean a viable and sustainable solution for the mitigation of environmental pollution.

2. Materials and Methods

2.1. Study Area

This research was carried out in Ecuador, Chimborazo province, Guamote canton, Reten community, covering an area of 4485.21 hectares, located in the micro-watershed of the Cebadas river, coordinates 2°06′00.9″ S 78°31′14.9″ W (Figure 1). The study focused on the high-altitude paramo ecosystem with an altitudinal range from 3300 to 3600 m above sea level. The predominant vegetation of this ecosystem corresponds to grasses and herbs [24]. It has a temperature ranging between 4 and 12 °C and average annual rainfall between 250 mm and 2500 mm [25].

2.2. Sampling, Collection, and Identification of Plant Species

The sample size formula was used for a finite population. A margin of error of 5% and a confidence level of 95% were considered. The formula is as follows:

$$\mathrm{n}={\displaystyle \frac{\mathrm{N}(\mathrm{p}\times \mathrm{q})}{\left(\mathrm{N}-1\right)({\frac{\mathrm{e}}{\mathrm{z}})}^2+(\mathrm{p}\times \mathrm{q})}}$$

where N is the universe or population (50), p is the occurrence (0.5), q is the non-occurrence (0.5), e is the error (0.05), z is the confidence level (1.96), and n is the sample size (45). Using the Fishnet tool from ArcToolBox-Data Management Tools-Sam-pling-Create Fishnet of ArcGIS software version 10.8, 45 sampling units of 1000 m × 1000 m were generated.

For the inventory and collection of plant species, the Gloria method (Global Observation Research Initiative in Alpine Environments) was used, adapted for Andean moorlands [26], because the study area corresponds to herbaceous vegetation; quadrants of 1 m² (1 × 1 m) were established in each plot analyzed. Subsequently, during the observation phase, the recording and counting of plant species were carried out only in the extreme quadrants, since the rest could have been altered by the trampling of the researchers.

The collected samples were placed on sheets of filter paper for one week to remove moisture. The paper was constantly checked and changed to avoid decomposition of the specimens. Subsequently, the samples were pressed and placed in orderly layers, wrapped in filter paper and cardboard to form a pile. Finally, the dried samples were placed on white cardboard for identification in the database of the Espoch–Herbarium repository (Figure 2).

The identification was validated through the use of virtual identification resources such as the Global Biodiversity Information Facility (GBIF) repository, the Tropics herbarium, and the Austral Americano herbarium. With the taxonomic identification of the species, we proceeded to calculate the importance value index (IVI) corresponding to a key metric in floristic studies because it shows the importance and relevance of a species within a plant community, as well as its ecological dominance in relation to the rest of the vegetation [27,28]. The following formula was used [29,30]:

$$\mathrm{IVI}={\displaystyle \frac{DnR+FR}{2}}$$

where DnR is the relative density, FR is the relative frequency, and IVI is the importance value index.

2.3. Metal Analysis by Spectrometry

The methodology used followed the international standards of the Environmental Protection Agency (EPA). For this purpose, the specific part of each species to be analyzed (root, stem, and leaves) was identified. Nitrile gloves and stainless steel scissors sterilized with alcohol were used. Three samples per species and vegetative organ were collected, avoiding contact with the soil or contaminating particles. The samples were cleaned and stored in airtight bags. They were labeled and transported in a cooler. For the analysis of heavy metals, the Inductively Coupled Plasma Atomic Emission Spectrometry (ICP-AES) method was used, which is an effective technique for determining the elemental composition of a sample [31,32,33].

The plant samples were separated according to their vegetative organs: root, stem, and leaves. They were then washed with distilled water, dried at 60 °C in an oven until constant weight was reached, and subsequently ground to obtain a homogeneous powder. A closed microwave oven at high pressure and temperature was used for the acid digestion to ensure complete and safe digestion. Approximately 0.5 g of dry sample was weighed, to which 10 mL of high-purity nitric acid (HNO₃) was added. The procedure lasted approximately 6 h, distributed in 4 digestion stages. The accuracy of the analysis was verified with the elaboration of duplicates and the use of certified standards. The digested solution was introduced into a plasma composed of argon, which excited the atoms and ions to emit light at wavelengths.

Finally, a spectrometer measured the intensity of the light emitted, and from the intensity, the concentration of the elements in each plant sample was determined. In addition, the PE/AL/17 EPA 200.7 ICP-AES Rev.4.4 1994 method was used, which is a standardized analytical technique for the determination of the elements present in plants. In this way, the presence of heavy metals was quantified: cadmium (Cd), chromium (Cr), lead (Pb), mercury (Hg), silicon (Si), arsenic (As), and sodium (Na), since these metals are highly toxic in high concentrations [34]. Standards with a concentration of 1000 µg/mL in 2–5% nitric acid were taken into account, within the classification 17,034 certified reference material. It is worth mentioning that the concentrations of each standard vary according to the metal analyzed.

2.4. Translocation Factor

The translocation factor (TF), which evaluates the potential of a plant for phytoremediation, was determined and is defined as the quotient between the concentration of a specific metal in the aerial organs and the root [34,35,36]. The following equation was used to calculate the plant’s capacity to mobilize metals from roots to shoots:

$$TF={\displaystyle \frac{\mathrm{M}\mathrm{e}\mathrm{t}\mathrm{a}\mathrm{l} \mathrm{c}\mathrm{o}\mathrm{n}\mathrm{c}\mathrm{e}\mathrm{n}\mathrm{t}\mathrm{r}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{o}\mathrm{n} \mathrm{i}\mathrm{n} \mathrm{a}\mathrm{e}\mathrm{r}\mathrm{i}\mathrm{a}\mathrm{l} \mathrm{p}\mathrm{a}\mathrm{r}\mathrm{t}\mathrm{s}}{\mathrm{M}\mathrm{e}\mathrm{t}\mathrm{a}\mathrm{l} \mathrm{c}\mathrm{o}\mathrm{n}\mathrm{c}\mathrm{e}\mathrm{n}\mathrm{t}\mathrm{r}\mathrm{a}\mathrm{t}\mathrm{i}\mathrm{o}\mathrm{n} \mathrm{i}\mathrm{n} \mathrm{r}\mathrm{o}\mathrm{o}\mathrm{t}}}$$

Translocation factors greater than 1 indicate the greater capacity of a specific plant to transport metals from the roots to the shoots, while values less than 1 indicate that the metal is stored or stabilized in the roots [18,37]. The plant is considered an accumulator if it obtains a TF equal to or greater than 1, but if it has the capacity to accumulate from 5 to 500 times more than the average, it is called a hyperaccumulator [38,39] (

Table 1. Translocation factor classification (FT).

Concentration (mg/kg)	Classification
FT > 1	Transfers (hyperaccumulator)
FT < 1	Stabilizes

Source: Baker, 1981 [41].

). This factor has no units but can be represented in percentages [40].

2.5. Cluster Analysis

Cluster analysis, used to classify and interpret complex data in plant composition research, was applied to identify patterns [42]. The availability of advanced multivariate statistical techniques enhances the identification of homogeneous groups in environmental data. Cluster analysis has been key in the identification of hyperaccumulating plants [43,44]. The correlation clustering method was used, and considering that rij is the Pearson correlation coefficient between two variables or observations i and j, the dissimilarity (or distance) measure is expressed as:

Dij = 1 − rij

where rij is the Pearson correlation between i and j, and dij is the distance based on the correlation.

3. Results

3.1. Floristic Inventory Importance Value Index (IVI)

A total of 24 families, 41 genera, and 43 species were identified (

Table 2. Floristic Inventory.

Family	Species	Family	Species	Family	Specie
Apiaceae	Azorella pedunculata	Bryaceae	Bryaceae	Lamiaceae	Clinopodium nubigenum
Apiaceae	Daucus montanus	Caprifoliaceae	Valeriana microphylla	Lamiaceae	Stachys elliptica
Apiaceae	Hydrocotyle bonplandii	Caryophyllaceae	Drymaria ovata	Lycopodiaceae	Huperzia crassa
Asteraceae	Bidens andicola	Cyperaceae	Eleocharis	Peltigeraceae	Peltigera
Asteraceae	Diplostephium glandulosum	Cyperaceae	Carex bonplandii	Plantaginaceae	Plantago australis
Asteraceae	Baccharis genistelloides	Dryopteridaceae	Polystichum orbiculatum	Poaceae	Calamagrostis intermedia
Asteraceae	Hypochaeris sessiliflora	Dryopteridaceae	Elaphoglossum cuspidatum	Poaceae	Agrostis perennnans
Asteraceae	Gnaphalium	Ericaceae	Pernettya prostrata	Poaceae	Agrostis breviculmis
Asteraceae	Lasiocephalus ovatus	Fabaceae	Vicia andicola	Polygonaceae	Rumex acetocella
Asteraceae	Baccharis salicifolia	Fabaceae	Trifolium repens	Ranunculaceae	Ranunculus praemorsus
Asteraceae	Gynoxys sp.	Gentianaceae	Halenia weddeliana	Rosaceae	Acaena ovalifolia
Asteraceae	Monticalia arbutifolia	Gentianaceae	Gentiana sedifolia	Rosaceae	Lachemilla orbiculata
Asteraceae	Taraxacum officinale	Geraniaceae	Geranium laxicaule	Equisetaceae	Equisetum bogotense
Bartramiaceae	Breutelia tomentosa	Gunneraceae	Gunnera magellanica
Brassicaceae	Nasturtium officinale	Iridaceae	Orthrosanthus chimboracensis

). The Asteraceae family recorded 10 species: Bidens andicola, Diplostephium glandulosum, Baccharis genistelloides, Hypochaeris sessiliflora, Gnaphalium, Lasiocephalus ovatus, Baccharis salici-folia, Gynoxys sp., Monticalia arbutifolia, and Taraxacum officinale. It is a family with great floristic richness and possesses favorable biological characteristics for its adaptation to different environments [45,46]. The Poaceae family also stands out because it can expand in aquatic and terrestrial environments due to the morphological adaptations it possesses. They are grasses used in soil stabilization and carbon sequestration, which contributes to climate change mitigation [47]. Similarly, the Apiaceae family is recognized for its morphological and physiological characteristics that facilitate its use in the bioremediation of contaminated soils [48].

In addition, the Agrostis genus is one of the most diverse in the world [49], with the species A. perennnans and A. breviculmis, while the Baccharis genus includes B. genistelloides and B. salicifolia.

On the other hand, the species Carex bonplandii and Eleocharis sp. stand out, included in the Cyperaceae family that comprises approximately 5000 species around the world, which shows their ecological and economic importance [50].

Twelve plant species with the highest importance value indexes were determined. The species Calamagrostis intermedia of the Poaceae family registered 9217 individuals, being the family with the highest number of individuals registered and an importance value index of 31.09% of the total cover, followed by the species Lachemilla orbiculata with 4481 individuals (18.06%), and Plantago australis with 937 individuals (7.56%). These species stand out for their ecological dominance and their importance in the vegetation cover of the area under study (

Table 3. Importance value index (IVI).

Family	Species	Individuals	Frequency	Relative Density%	Relative Frequency%	IVI%
Poaceae	Calamagrostis intermedia	9217	42	51.21	10.97	31.09
Rosaceae	Lachemilla orbiculata	4481	43	24.89	11.23	18.06
Plantaginaceae	Plantago australis	937	38	5.21	9.92	7.56
Polygonaceae	Rumex acetocella	669	31	3.72	8.09	5.91
Cyperaceae	Carex bonplandii	436	29	2.42	7.57	5.00
Lamiaceae	Clinopodium nubigenum	667	24	3.71	6.27	4.99
Equisetaceae	Equisetum bogotense	160	22	0.89	5.74	3.32
Cyperaceae	Eleocharis sp.	222	20	1.23	5.22	3.23
Asteraceae	Taraxacum officinale	181	20	1.01	5.22	3.11
Ericaceae	Pernettya prostrata	111	21	0.62	5.48	3.05
Asteraceae	Baccharis salicifolia	189	11	1.05	2.87	1.96
Asteraceae	Gynoxys buxifolia	96	8	0.53	2.09	1.31

).

Below are photographs taken in the field of the vegetative species Calamagrostis intermedia, Lachemilla orbiculata, Plantago australis Lam, Clinopodium nubigenum (Kunth), Taraxacum officinale Weber, Carex bonplandii Kunth, Pernettya prostrata (Cav.), Baccharis salicifolia, Eleocharis sp., Rumex acetocella L., Gynoxys buxifolia (Kunth), and Equisetum bogotense (Figure 3). The aforementioned species are of high ecological importance and have morphological and physiological adaptations that allow them to adapt to different environments, which is essential for them to be considered species with phytoremediating capacity.

3.2. Metal Analysis by Spectrometry

It was determined that, in high Andean plants, the average cadmium content (1.93 mg/kg) is significantly higher than in lowland plants, where it is typically less than 0.2 mg/kg. Thus, the 12 species analyzed presented cadmium in their roots, stems, and leaves, which reflects the capacity of high Andean species to tolerate and accumulate this heavy metal in their tissues due to the geological composition of the soil. Lead presented low values in roots, stems, and leaves, ranging from 0.01 mg/kg (Rumex acetocella L.) to 0.43 mg/kg (Plantago australis) (

Table 4. Presence of metals in the root, stem, and leaves of high Andean plant species.

Heavy Metals	Plant Species	Lachemilla orbiculata	Carex bonplandii	Baccharis salicifolia	Taraxacum officinale	Pernettya postrata	Equisetum bogotense	Rumex acetocella L.	Calamagrostis intermedia	Eleocharis sp.	Plantago australis	Clinopodium Nubigenum	Gynoxys sp.
Cadmium	root	0.50	0.14	0.14	2.17	0.19	1.20	0.16	0.14	0.21	0.13	0.78	0.64
	stem	1.04	0.60	10.61	1.62	0.38	0.13	0.94	5.23	0.14	1.40	0.52	0.53
	leaves	0.55	0.38	12.01	2.05	0.66	0.41	1.10	0.93	3.47	1.21	0.51	7.23
Chromium	root	0.00	21.88	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00
	stem	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00
	leaves	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00
Lead	root	0.03	0.02	0.00	0.44	0.03	0.02	0.01	0.10	0.16	0.00	0.26	0.13
	stem	0.19	0.10	0.13	0.40	0.04	0.00	0.07	0.03	0.00	0.43	0.19	0.09
	leaves	0.12	0.06	0.29	0.39	0.10	0.04	0.13	0.11	0.06	0.13	0.11	0.14
Mercury	root	1.31	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00
	stem	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00
	leaves	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00
Silicon	root	300.00	280.00	320.00	250.00	348.00	324.80	371.20	290.00	403.68	376.77	430.59	336.40
	stem	250.00	310.00	370.00	220.00	290.00	359.60	429.20	255.20	336.40	417.14	497.87	296.03
	leaves	350.00	240.00	230.00	300.00	406.00	278.40	266.80	348.00	470.96	322.94	309.49	403.68
Arsenic	root	1.91	1.99	2.22	2.46	2.59	3.67	2.93	3.20	3.18	3.18	3.34	3.35
	stem	1.84	2.09	2.37	2.48	2.55	3.11	2.90	3.04	3.19	3.22	3.26	3.38
	leaves	1.93	2.11	2.33	2.57	2.61	2.89	2.99	3.04	3.13	3.19	3.29	3.35
Sodium	root	951.07	54.53	0.00	0.00	21.21	0.00	0.00	0.00	0.00	0.00	0.00	0.00
	stem	513.02	25.30	0.00	0.00	21.21	0.00	0.00	0.00	0.00	0.00	0.00	0.00
	leaves	98.68	0.00	0.00	19.88	0.00	0.00	0.00	0.00	0.00	0.00	0.00	0.00

).

The average silicon content in the stems (335.95 mg/kg) was high, with a maximum of 497.87 mg/kg (Clinopodium nubigenum). High levels of silicon were found in the roots, stems, and leaves of all the species analyzed, due to the fact that silicon is the second most abundant element, and that it is formed by the weathering of volcanic ash. This element contributes to resistance to biotic and abiotic stress, such as drought and low temperatures, which is characteristic of the Andean zone.

Arsenic averaged 2.79 mg/kg, which is much higher than in lowland plants, where it is usually less than 0.5 mg/kg. The high concentration could be due to the volcanic geology and heavy metal-rich soils of the Andes.

On the other hand, Carex bonplandii was the only species to present chromium (21.88 mg/kg) in its roots, and mercury (1.31 mg/kg) was also determined in the roots of Lachemilla orbiculata.

Sodium was recorded only in the species Lachemilla orbiculata, in the root (951.07 mg/kg), stem (513.02 mg/kg), and leaves (98.68 mg/kg); Carex bonplandii root (54.53 mg/kg) and stem (25.30 mg/kg); Taraxacum officinale leaves (19.88 mg/kg); and Pernettya prostrata root (21.21 mg/kg) and stem (21.21 mg/kg) (Table 4).

3.3. Translocation Factor

The species Lachemilla orbiculata, Carex bonplandii, Pernettya prostrata, Equisetum bogotense, Rumex acetocella L., Calamagrostis intermedia and Gynoxys sp. were determined as hyperaccumulators of lead in leaves, while Taraxacum officinale, Eleocharis sp., and Clinopodium nubigenum were defined as lead-stabilizing species in their roots. On the other hand, arsenic, being a dangerous contaminant, was observed in Lachemilla orbiculata, Carex bonplandii, Baccharis salicifolia, Taraxacum officinale, Pernettya prostrata, Rumex acetocella L., Plantago australis, and Gynoxys sp., resulting in hyperaccumulator species of this metal in leaves, while the species Equisetum bogotense, Calamagrostis intermedia, Eleocharis sp., and Clinopodium nubigenum stabilize the metal in the root (

Table 5. Translocation factor leaves/roots.

Species	Heavy Metal Leaves/Roots (mg/kg)
	Cd	Cr	Pb	Hg	Si	As	Na
Lachemilla orbiculata	1.11	0.00	4.01	0.00	1.17	1.01	0.10
Carex bonplandii	2.77	0.00	3.53	0.00	0.86	1.06	0.00
Baccharis salicifolia	86.28	0.00	0.00	0.00	0.72	1.05	0.00
Taraxacum officinale	0.95	0.00	0.88	0.00	1.20	1.05	0.00
Pernettya prostrata	3.56	0.00	3.55	0.00	1.17	1.01	0.00
Equisetum bogotense	0.34	0.00	1.66	0.00	0.86	0.79	0.00
Rumex acetocella L.	6.93	0.00	9.27	0.00	0.72	1.02	0.00
Calamagrostis intermedia	6.59	0.00	1.12	0.00	1.20	0.95	0.00
Eleocharis sp.	16.50	0.00	0.36	0.00	1.17	0.98	0.00
Plantago australis	9.01	0.00	0.00	0.00	0.86	1.00	0.00
Clinopodium nubigenum	0.66	0.00	0.40	0.00	0.72	0.99	0.00
Gynoxys sp.	11.22	0.00	1.12	0.00	1.20	1.00	0.00

), due to the transfer of these elements from the root.

According to the translocation factor stem/root ratio, high values were observed in the species Baccharis salicifolia (76.17%) and Calamagrostis intermedia (37.16%), which are determined as species that hyperaccumulate cadmium in the stem, followed by Plantago australis, Rumex acetocella L., Carex bonplandii, Pernettya prostrata, and Lachemilla orbiculata, with a translocation factor greater than 1. The species with the lowest translocation factor, and therefore a translocation factor less than 1, was Calamagrostis intermedia, which stabilizes the lead in its root without translocating or mobilizing it to the rest of the vegetative organs of the plant. On the other hand, values of zero were determined for chromium and mercury (

Table 6. Stem/root translocation factor.

Species	Heavy Metal Stem/Root (mg/kg)
	Cd	Cr	Pb	Hg	Si	As	Na
Lachemilla orbiculata	2.08	0.00	6.50	0.00	0.83	0.96	0.54
Carex bonplandii	4.38	0.00	5.76	0.00	1.11	1.05	0.46
Baccharis salicifolia	76.17	0.00	0.00	0.00	1.16	1.07	0.00
Taraxacum officinale	0.75	0.00	0.91	0.00	0.88	1.01	0.00
Pernettya prostrata	2.02	0.00	1.42	0.00	0.83	0.99	1.00
Equisetum bogotense	0.11	0.00	0.00	0.00	1.11	0.85	0.00
Rumex acetocella L.	5.90	0.00	4.96	0.00	1.16	0.99	0.00
Calamagrostis intermedia	37.16	0.00	0.29	0.00	0.88	0.95	0.00
Eleocharis sp.	0.67	0.00	0.00	0.00	0.83	1.00	0.00
Plantago australis	10.45	0.00	0.00	0.00	1.11	1.01	0.00
Clinopodium nubigenum	0.67	0.00	0.71	0.00	1.16	0.98	0.00
Gynoxys sp.	0.82	0.00	0.72	0.00	0.88	1.01	0.00

).

3.4. Cluster Analysis

Group 1 is visually marked by the cluster of elements on the right (Lead TR/HR, Sodium TR/HR), and by high values (green/yellow cells). This group, highlighting a close relationship between lead and sodium in moorland plant species, reflects complex physiological and ecological interactions. While sodium is essential for osmotic regulation and can substitute for potassium in deficiency conditions [51,52], it is also a highly toxic metal that can alter nutrient absorption and generate ionic imbalances [53].

The negative correlation between silicon (Si) and cadmium (Cd) translocation in Baccharis salicifolia is due to the ability of silicon to mitigate cadmium toxicity by reducing its uptake and mobility within the plant.

Group 2 is marked by the cluster of elements in the middle-left part (arsenic TR/HR, cadmium TR/HR) and by the patterns of values (green and red, with some yellow cells). This group presented an interaction between arsenic and cadmium due to their availability in the soil, absorption mechanisms, and physiological responses to heavy metal stress. Both elements are mobilized under similar environmental conditions, such as variations in soil pH and humidity, which favors their joint absorption in paramo ecosystems [54,55]. Their toxicity can generate synergistic interactions that affect the accumulation and detoxification of each metal [56,57,58] (Figure 4).

With respect to the species, two groups were identified, in which the first was characterized by a positive relationship for the translocation of silicon from root to stem, and the second had a negative relationship. The translocation of silicon from root to stem in paramo plants is regulated by physiological and genetic mechanisms that optimize its absorption and distribution. Silicon is transported to aerial tissues by genes such as Lsi1, Lsi2, and Lsi6, which facilitate its mobility and accumulation in leaves and stems, strengthening their mechanical resistance and tolerance to environmental stress [59,60,61] (Figure 4).

4. Discussion

4.1. Floristic Diversity-Importance Value Index (IVI)

Studies developed in the Ilo-Moquegua and Lomas de Ilo River basin and the Pomacocha and Habascocha Andean lagoons in Peru determined a significant contribution of the Poaceae and Asteraceae families to the local floristic diversity, representing about 51% of the vegetation cover. These families occupy the first places in dominance in high mountain ecosystems [62,63,64], provide habitats, and contribute to the capacity of species to adapt to environmental changes.

Poaceae are crucial for soil stabilization in areas prone to erosion, which allows them to proliferate in aquatic and terrestrial environments to maintain water quality and prevent flooding [47,65]. Their physiology allows the accumulation of biomass and therefore the conservation of carbon in the soil [66].

Species of the Asteraceae family are considered indicators of ecosystem health and richness [67]. They are essential for global ecology due to their high diversity, adaptability, and role as an indicator of ecological health that contributes to vegetation restoration and biodiversity conservation [45,62,68,69]. The species under study are of high ecological importance due to their great contribution to biodiversity and ecosystem stability, which makes their preservation indispensable for environmental sustainability.

4.2. Translocation Factor

Heavy metals generally accumulate first in the roots and are later redistributed to the aerial parts of the plant [70,71].

In the present study, the translocation of cadmium (Cd) and arsenic (As) in Baccharis salicifolia is highlighted as a key factor in phytoremediation. Cadmium, being highly mobile, reaches translocation factors (TF) higher than 1, which indicates its potential for metal accumulation in the aerial part of the plant [72,73]. It has also been determined that the translocation of lead and sodium has consequences in the tolerance to stress due to heavy metals, which is influenced by environmental factors [74,75]. Research has shown that the vascular mobilization of arsenic is carried out by specific transporters [76,77,78]. Previous studies have shown that silicon forms apoplastic barriers in the roots and reduces the rate of transpiration, which limits the entry of cadmium and therefore reduces its concentration in the shoots, and also indicates that it may alter the efficient transport of cadmium, with these interactions being more complex. These data suggest that silicon is a key element to counteract cadmium accumulation [79,80,81,82]. It is worth mentioning that the physiological stress caused by the accumulation and toxicity of metals can cause cellular damage in the plant, so to face this challenge, high Andean vegetation has developed protection mechanisms, such as the production of certain proteins that can bind to metals and antioxidants to reduce their toxicity. Thus, phytoextraction has been an effective and recognized mechanism, due to the interaction of plants with microorganisms that facilitate the availability and absorption of heavy metals by their root system to be transported to the leaves [83].

4.3. Cluster Analysis

Studies carried out by Mukhomorov [84] and Meleshko et al. [85] showed that the content of chemical elements in plants allows the formation of associations and significant interactions, which is why they used this guide to develop composition models in edible plants. Similarly, Alekseenko et al. [86] and Zuluaga et al. [87] analyzed the accumulation of metals using inductively coupled plasma mass spectrometry, where they pointed out the great importance of precise analytical methods for obtaining real data.

On the other hand, several investigations [88,89] have shown that high concentrations of heavy metals in Andean soils are a consequence of the development of human activities that cause health threats.

It should be noted that the solubility and transport of heavy metals in the soil are influenced by environmental conditions [90]. Thus, the higher the altitude, the higher the mineral content (essential nutrients/heavy metals) of the soil, which can also influence the absorption of nutrients [91,92]. This agrees with research carried out in several countries [93,94,95,96]. where it is pointed out that plant species at higher altitudes produce as a defense mechanism metabolites that generate a higher concentration of cadmium and arsenic in the tissues, which in turn facilitates the accumulation of nutrients and metals [97]. It is worth mentioning that the roots possess mycorrhizal fungi that function as metal transporters [91,92,98,99], which facilitate the accumulation of nutrients and metals, allowing their bioavailability in the soil [97]. This is essential for the stabilization of metals and restricts the translocation of metals to the aerial part of the plant [88,100]. The presence of lead caused by anthropogenic activities could affect the bioavailability of sodium; this has been evidenced in high Andean soils with low content of this element, which directly influences the nutrition of plant resources [101,102]. Therefore, it is essential to understand the interactions between elements in order to evaluate the environmental impact of plant physiology and the balance of ecosystems [103,104].

On the other hand, several investigations have determined that arsenic and cadmium toxicity can generate synergistic interactions, affecting the accumulation and detoxification of each metal [56,57,58]. However, certain species of the paramo have developed optimal genetic adaptations that increase tolerance to contamination [105].

Studies carried out in Mexico and Brazil have determined that the accumulation of silicon significantly improves plant response to drought, salinity, and metal contamination, and also reduces the toxicity of contaminants such as arsenic [106,107], while its interaction with other nutrients such as phosphorus and potassium allows adequate plant development [108,109].

High Andean vegetation has certain physiological adaptations that allow greater accumulation of nutrients and metals [110,111]. The presence of specific transporters in the roots is of vital importance in the stabilization and translocation of metals to the aerial part of the plant [88,99,100]. In addition, it has been observed that plants at higher altitudes have a large amount of root biomass that allows greater absorption of elements [112]. It has also been determined that the interaction between altitude and climate directly influences the accumulation of metals in the roots of plants. Thus, Thakur et al. 2019 point out that increased solar radiation can stimulate photosynthesis and the production of organic compounds that could accumulate heavy metals in plant tissues [113].

5. Conclusions

In the present study, the Poaceae (51.59%) and Rosaceae (24.95%) families were identified as having the greatest plant coverage, while Asteraceae stood out for its diversity of species. The plant species Lachemilla orbiculata, Carex bonplandii, Vaccinium floribundum, Baccharis salicifolia, Taraxacum officinale, Pernettya prostrata, Equisetum bogotense, Rumex acetocella L., Calamagrostis intermedia, Nasturtium officinale R. Br, Eleocharis sp., and Plantago australis were determined as hyperaccumulators and stabilizers of cadmium, lead, and arsenic, which are considered highly toxic to the health of the population and the environment.

Of the plant species identified, Baccharis salicifolia (76.17%) and Calamagrostis intermedia (37.16%) had high rates of cadmium translocation from roots to stems and leaves, while Lachemilla orbiculata was found to be a sodium stabilizer. However, Calamagrostis intermedia also showed root stabilization of lead.

High Andean native plant species have great potential for phytoremediation, not only because of their capacity to accumulate heavy metals, but also because of their physiological adaptations to optimize nutrient and heavy metal uptake. Therefore, research is crucial for the development of effective remediation strategies that contribute to the restoration of contaminated ecosystems.

Technical and scientific knowledge about high Andean plant species in the absorption and translocation of heavy metals allows the creation of environmental regulations and programs for the restoration of high Andean ecosystems, which increases the ecological value of the area under study. In addition, the preservation of the species promotes the generation of low-cost and ecological solutions for the long-term protection of ecosystems.