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Article

Assessment of Heavy Metal Transfer from Soil to Forage and Milk in the Tungurahua Volcano Area, Ecuador

by
Lourdes Carrera-Beltrán
1,
Irene Gavilanes-Terán
1,
Víctor Hugo Valverde-Orozco
2,
Steven Ramos-Romero
3,
Concepción Paredes
3,
Ángel A. Carbonell-Barrachina
3 and
Antonio J. Signes-Pastor
3,4,5,6,*
1
Facultad de Ciencias, Escuela Superior Politécnica de Chimborazo (ESPOCH), Riobamba 060155, Ecuador
2
Facultad de Ingeniería, Universidad Nacional de Chimborazo, Riobamba 060108, Ecuador
3
Centro de Investigación e Innovación Agroalimentaria y Agroambiental (CIAGRO-UMH), Miguel Hernández University, EPSO-Orihuela, Ctra. Beniel km 3.2, Orihuela, 03312 Alicante, Spain
4
Unidad de Epidemiología de la Nutrición, Universidad Miguel Hernández, 03550 Sant Joan d’Alacant, Spain
5
CIBER de Epidemiología y Salud Pública (CIBERESP), Instituto de Salud Carlos III (ISCIII), 28029 Madrid, Spain
6
Instituto de Investigación Sanitaria y Biomédica de Alicante (ISABIAL), 03010 Alicante, Spain
*
Author to whom correspondence should be addressed.
Agriculture 2025, 15(19), 2072; https://doi.org/10.3390/agriculture15192072
Submission received: 25 August 2025 / Revised: 29 September 2025 / Accepted: 30 September 2025 / Published: 2 October 2025
(This article belongs to the Section Agricultural Soils)

Abstract

The Bilbao parish, located on the slopes of the Tungurahua volcano (Ecuador), was heavily impacted by ashfall during eruptions between 1999 and 2016. Volcanic ash may contain toxic metals such as Pb, Cd, Hg, As, and Se, which are linked to neurological, renal, skeletal, pulmonary, and dermatological disorders. This study evaluated metal concentrations in soil (40–50 cm depth, corresponding to the rooting zone of forage grasses), forage (English ryegrass and Kikuyu grass), and raw milk to assess potential risks to livestock and human health. Sixteen georeferenced sites were selected using a simple random probabilistic sampling method considering geological variability, vegetation cover, accessibility, and cattle presence. Samples were digested and analyzed with a SpectrAA 220 atomic absorption spectrophotometer (Varian Inc., Victoria, Australia). Soils (Andisols) contained Hg (1.82 mg/kg), Cd (0.36 mg/kg), As (1.36 mg/kg), Pb (1.62 mg/kg), and Se (1.39 mg/kg); all were below the Ecuadorian limits, except for Hg and Se. Forage exceeded FAO thresholds for Pb, Cd, As, Hg, and Se. Milk contained Pb, Cd, and Hg below detection limits, while Se averaged 0.047 mg/kg, exceeding water safety guidelines. Findings suggest soils act as sources with significant bioaccumulation in forage but limited transfer to milk. Although immediate consumer risk is low, forage contamination highlights long-term hazards, emphasizing the need for monitoring, soil management, and farmer guidance.

1. Introduction

Volcanic eruptions are one of the primary natural sources of environmental pollutants, directly affecting human populations, their livelihoods, and local economies. The consequences of such eruptions are observable at a local scale and may extend globally [1]. It is estimated that between 30 and 800 million people live within a radius of 10 to 100 km of active volcanoes worldwide [2]. For communities residing in close proximity (~10 km), volcanic activity poses a significant risk due to the dispersion of tephra, pyroclastic events, and the social impacts associated with perceived vulnerability and the variability of eruptive behavior [3,4]. Various studies have indicated that eruptions influence the atmosphere both in nearby regions [5] and at distances of thousands of kilometers [6], highlighting the magnitude and far-reaching effects of these natural processes.
In Ecuador, the prolonged eruption of the Tungurahua volcano between 1999 and 2016 had severe repercussions on local agriculture and livestock production. The continuous deposition of volcanic ash led to significant alterations to soil properties, including increased sulfur content and soil acidification, which reduced the bioavailability of essential nutrients for crops and pastures. These effects were further exacerbated by the intrinsic characteristics of the region’s soils, marked by low organic matter content and reduced pH levels. Such conditions promote the solubilization and availability of heavy metals while simultaneously limiting the formation of stable organometallic complexes that could otherwise be absorbed by plants through their root systems [7,8].
During the initial years of the eruption, ash deposits of up to one meter in depth were recorded in nearby areas, severely affecting agricultural and livestock systems [1,9]. Traditional crops such as maize, tomato, and beans experienced a drastic decline, prompting a shift toward more resilient crops like maize and beans, as well as increased livestock production. However, livestock systems also experienced setbacks in growth, reproduction, and milk production, with some cases reporting animal mortality. These adverse effects were attributed to the high exchangeable acidity, elevated aluminum concentrations, and salinity of the volcanic ash, which negatively impacted forage species such as clover, oats, peas, and forage maize [9,10,11,12].
A key driver of these disruptions is the presence of inorganic compounds in volcanic ash, particularly toxic trace elements such as metals, heavy metals, and metalloids, including Pb, Cd, As, Cr, Cu, Hg, Ni, Sb, and Zn [13,14,15,16]. These elements can accumulate in soils, be absorbed by plants, and enter the food chain [17,18]. Their non-biodegradable nature and potential for bioaccumulation pose serious risks to ecosystems and human health [6,18,19,20]. For instance, Cd in high concentrations causes physiological damage in plants, including leaf wilting, reduced root length, and biomass [21]. Cadmium interferes with nitrogen and carbohydrate metabolism, inhibits photosynthesis, disrupts chlorophyll synthesis, and induces stomatal closure [22]. In humans, prolonged Cd exposure results in oxidative damage in blood and liver, as well as histopathological changes in renal, cerebral, and testicular tissues [22,23,24]. Lead similarly accumulates in plant organs at higher concentrations than in surrounding soils, reducing chlorophyll production and biomass while limiting growth due to decreased nitrogen availability [22]. In humans, Pb bioaccumulates through absorption and magnification, causing disruptions in neurological, skeletal, reproductive, hematopoietic, renal, and cardiovascular systems [25].
Arsenic also represents a global public health concern, as it is linked to increased cancer incidence, skin diseases, and cellular dysfunction. It disrupts cellular activity, induces abnormalities in inflammatory mechanisms, and impairs immune system function [26]. Mercury, another hazardous contaminant, causes environmental ecotoxicity and, in humans, leads to neurotoxic and neurological disorders, genotoxicity, immunogenicity, pregnancy complications, and reproductive system damage, with additional links to cancer promotion, cardiotoxicity, pulmonary diseases, and nephropathies [27,28]. Selenium, in contrast, exhibits a dual role. At low concentrations, it enhances plant growth and mitigates stress caused by toxic trace elements, while in humans, deficiency increases mortality risk, impairs immune function, and affects cognition and thyroid function. However, levels slightly above dietary requirements may cause neurological impairments and increase the risk of type 2 diabetes [14,29,30,31].
Understanding the movement of these metals in agricultural systems is therefore essential. Metal uptake by plants is commonly evaluated using the bioconcentration factor (BCF), which measures the accumulation of metals in roots relative to soil concentrations. A BCF > 1 suggests hyperaccumulation, while a BCF < 1 indicates exclusion [18,32,33,34]. The translocation factor (TF) quantifies the transport of metals from roots to shoots, with values > 1 indicating efficient internal movement. Once present in forage, metals may be ingested by grazing animals and transferred to products such as milk. This trophic transfer is assessed using the biotransfer factor (BTF), which relates metal concentrations in animal products to dietary levels. Excretion into milk follows first-order kinetics [32,34], making milk a key indicator of dietary metal exposure.
A preliminary field assessment identified the parish of Bilbao (Penipe Canton, Chimborazo Province) as one of the regions most affected by ashfall [35]. Preliminary interviews with local residents and authorities, conducted during community clean-up events organized in coordination with the local municipality, included 43 surveys from the parish center, Santa Cruz, and the communities of Chotapamba, Motilones, and Yuibug (Figure S1). Although not formally published, these observations suggested visible declines in crop and pasture quality, as well as concerns regarding the safety and appearance of locally produced milk—a vital dietary component and a potential pathway for human exposure to heavy metals. Despite these concerns, no prior studies have comprehensively evaluated the soil–plant–animal–milk pathway in this region. To address this gap, the present study evaluates heavy metal contamination in the Bilbao parish, where 16 sampling points were established for the collection of soil, forage, and raw milk samples. Specifically, it examines the physicochemical characteristics of soils, nutrient composition of forage and milk, and the concentrations of potentially toxic elements (Pb, Cd, As, Hg, and Se) across all matrices. Bioaccumulation and biotransfer models are then applied to estimate metal mobility through the food chain, while statistical analyses explore relationships between metal concentrations and physicochemical or nutritional variables. These models and correlations, however, are exploratory in nature and cannot establish definitive causal relationships between soil properties and metal transfer. This integrated approach nonetheless provides critical insights for assessing potential risks to animal and human health and for informing mitigation strategies in volcanic-impacted agricultural systems.

2. Materials and Methods

2.1. Study Area

This study was conducted in the Bilbao parish, located on the northern flank of the Tungurahua volcano in the central Andean region of Ecuador. Administratively, Bilbao belongs to Penipe Canton in Chimborazo Province, approximately 42 km southeast of Riobamba, and is situated between the central and western mountain ranges at approximately 1.44° S latitude and 78.50° W longitude. The region spans elevations from 2100 to 4900 m above sea level, with an average annual temperature of 15 °C (ranging from 6 °C to 24 °C), annual precipitation between 700 and 1000 mm, and relative humidity of 65–85%. These agroclimatic conditions favor forage growth, soil regeneration, and livestock production.
Bilbao is characterized by mixed agricultural practices, with a strong dependence on livestock. As of 2018, 705 hectares (28.2% of the parish’s land area) were dedicated to livestock farming, while 237 hectares (9.5%) supported agroforestry systems integrating crops and animals. Most pastures are well-drained and benefit from favorable conditions for forage conservation. Baseline surveys revealed that 56% of residents engage in both agriculture and livestock rearing, while 9% specialize exclusively in livestock. Cattle ownership varies widely: 40% of households owned 1–3 head, 26% had 7–10, and 11% reported more than 20. In terms of milk production, 42% of households produced 10–20 L per day, 23% produced 21–40 L, and nearly 20% reported daily yields exceeding 80 L.
Milk is also an important dietary component, with 44% of households consuming it one to two times per day. This dietary reliance highlights the importance of assessing milk as a potential route of human exposure to heavy metals released by volcanic activity in the region.

2.2. Sampling

A total of 16 georeferenced sampling points were selected across the Bilbao parish with support from local authorities and community input (Figure S2). Site selection was based on a simple random probabilistic sampling method, ensuring equal inclusion probability. Criteria included geological variability, vegetation cover, accessibility, and cattle presence. This approach is widely recognized for its efficiency and representativeness in environmental studies [36,37]. Sampling was conducted between December 2020 and August 2021 in the communities of Motilones, Centro Parroquial, Yuibug Grande and Chico, Chontapamba, and Santa Cruz (Figure S2). At each site, three types of samples were collected: soil, forage, and raw milk. Environmental data, such as temperature and relative humidity, were measured in situ with a thermohydrometer, while geographic coordinates were recorded with a precision GPS and later mapped using Google Maps Platform (Google Earth Pro (Versión 7.3.6.10201)). The resulting data are summarized in Table S1.
Milk samples were collected during both morning and afternoon milking sessions to obtain representative composites. After milking all producing cows, samples were placed in the owners’ refrigeration tanks and homogenized by session (morning or afternoon). This procedure followed the standard practices used by local dairy producers for milk commercialization within and outside the parish. Approximately 300 mL of raw milk was taken from each site, homogenized, and stored in sterile coded containers. Samples were transported under refrigeration (coolers with ice packs) and stored at 4 °C until analysis. All milk samples were prepared and analyzed according to the Ecuadorian Technical Standard [38]. Soil samples were collected as composites from a depth of 40–50 cm, corresponding to the rooting zone of forage grasses. At each location, three subsamples were combined into one composite sample (~2 kg). Although volcanic ash thickness was not measured, the selected depth is considered appropriate for assessing root-zone contamination [39].
Forage samples consisted mainly of English ryegrass (Lolium perenne) and Kikuyu grass (Cenchrus clandestinus). Whole plants, including roots and aerial parts, were harvested and homogenized into composite samples (~2 kg per site). The collected mass was within acceptable analytical limits, although slightly below the benchmark proposed by [40].

2.3. Sample Preparation and Analysis

Soil and plant samples were prepared according to protocols described in previous studies [35,41,42]. Milk samples were filtered using a plastic sieve, heated to approximately 20 °C, and homogenized for subsequent analysis using LACTOSCAN equipment (Milkotronic Ltd., Nova Zagora, Bulgaria). For heavy metal analysis, milk samples were first digested in concentrated HNO3 (v/v; 1:2) at room temperature for 12 h. Distilled water was then added at a milk-to-water ratio of 1:4. The mixture was then digested at 100 °C until the volume was reduced to one-third. An equal volume of concentrated HCl and distilled water was added, followed by a second digestion step until the solution was reduced to one-third of its volume or until a clear digestate was obtained. The final solution was then filtered and analyzed. The digestion method was adapted from previous studies [43,44,45,46].

2.4. Physicochemical Analysis

The physicochemical and chemical analyses of soil and plant samples were performed following protocols described in previous studies [35,41]. For soils, parameters such as pH, electrical conductivity (EC), organic matter (OM), bulk density, true density, and texture were determined, along with macronutrients including P, K, N, and C. Phosphorus and potassium were obtained through acid digestion with H2SO4 [47]; P was measured by UV-VIS spectrophotometry and K by flame photometer. Nitrogen and carbon in soils and forage were analyzed using a direct combustion elemental analyzer (EUROVECTOR EA3000 - EuroVector S.r.l., Italy). In plant samples, pH, EC, OM, and Na, K, and P concentrations were determined. For milk samples, quality parameters were analyzed according to Ecuadorian technical standards, including pH (NTE INEN 1500:2011), density (NTE INEN 11), corrected density (Dcorr), fat (NTE INEN 12), total solids (TS; NTE INEN 14), protein (NTE INEN 16), solids-not-fat (SNG; NTE INEN 14), lactose (LACTOSCAN), freezing point (NTE INEN 15), salts (NTE INEN 14—ashes), and electrical conductivity.
To evaluate macro- and micro-nutrients as well as heavy metals, soil and plant samples were subjected to calcination–wet digestion using nitric acid (HNO3, 65%) at a 1:20 ratio. Concentrations of Pb, Cd, Hg, As, and Se were quantified in digested soil, plant, and milk samples with a SpectrAA 220 atomic absorption spectrophotometer (Varian Inc., Victoria, Australia), following established protocols [35,41,46,48]. Analytical accuracy was ensured through the use of blanks, replicates, and spiked samples, with recovery rates consistently near 100%. Detection limits (LOD) were calculated as the mean blank concentration plus three times the standard deviation, adjusted by dilution factor: for soils and forage, 10 mg/kg for Pb, 0.5 mg/kg for Cd, 0.075 mg/kg for As, 0.3 mg/kg for Se, and 0.1 mg/kg for Hg; for milk, 0.01 mg/kg for Pb, 0.2 mg/kg for Cd, 0.01 mg/kg for As, 0.12 mg/kg for Se, and 0.04 mg/kg for Hg. To assess metal dynamics across the soil–plant–animal–milk continuum, four indices were calculated: the root bioconcentration factor (BCF, Equation (1)), the aerial part bioaccumulation factor (BAF, Equation (2)), the translocation factor (TF, Equation (3)), and the biotransfer factor (BTF, Equation (4)) [18,32,33,49], with their mathematical equations (Eq.) presented below.
BCF = Metal   concentration Root Metal   concentration Soil
BAF = Metal   concentration Aerial   part Metal   concentration Soil
TF = Metal   concentration Edible   part Metal   concentration Root
BTF = Metal   concentration   in   milk / m g / k g 1 Average   daily   metal   consumption / m g / d a y 1
Together, these indices (Equations (1)–(4)) provide an integrated framework to assess metal uptake, internal distribution, translocation, and trophic transfer in volcanic-impacted agricultural systems, supporting both ecological risk assessments and the design of mitigation strategies.

2.5. Statistical Analysis

Physicochemical, nutrient, and toxic metal data from soil, plant, and milk samples across 16 sampling points were analyzed using descriptive statistics. Given the relatively small sample size, associations between heavy metal concentrations and physicochemical or nutrient parameters were assessed using the non-parametric Spearman rank correlation, which evaluates the strength and direction of monotonic relationships [50,51,52]. It should be emphasized that correlation analysis identifies associations but does not establish causation.

3. Results and Discussion

3.1. Physicochemical Parameters in Soil Samples

The results of the physicochemical analysis of soil samples are presented in Table S2. The soils exhibited a moderately acidic pH, characteristic of Andisols [53,54], and within the acceptable range for crop development [55]. Comparable values were reported by [56], although they were slightly higher than those observed by [7] in nearby areas. Electrical conductivity values indicated negligible salinity effects [53], consistent with findings by [7,56]. Organic matter (OM) content was classified as low [53] and was below the levels reported by [7,56]. Since OM plays a critical role in soil fertility, acting as a source of N, P, and K for plant growth, enhancing microbial activity, and improving soil structure, aeration, and moisture retention [57], these low values suggest potential limitations for crop and pasture productivity. The deposition of volcanic ash likely contributed to soil acidification, which, combined with low OM and reduced pH, may decrease nutrient availability while simultaneously increasing the solubility and mobility of heavy metals [7,8].
Regarding physical properties, soil texture was classified as sandy loam to loam, and bulk density values were within the acceptable range for soil quality as defined by [55]. These characteristics are consistent with those reported for weathered volcanic soils [54,56], supporting the classification of the studied soils as Andisols with inherent fertility and management challenges.

3.2. Soil Macronutrients

The results of the macronutrient analyses of the soils are presented in Table S3. The soils exhibited low concentrations of P (239.00–322.70 mg/kg) and K (734.76–1154.79 mg/kg), with values below 1200 mg/kg as defined by [17]. These levels are considerably lower than the adequate ranges suggested by [58], who recommend 10,000–50,000 mg/kg for K and 2000 mg/kg for P. The limited P availability may be linked to the soil pH values observed in the study (5.43–7.41), which restrict phosphorus solubility, together with the influence of volcanic ash on soil properties. In contrast, nitrogen levels were classified as rich to very rich (>0.30%), exceeding the reference range for cultivated soils (0.06–0.30%) reported by [57] and aligning with values typical of temperate to cold climate zones (0.02–1.06%). The coexistence of high N and low P concentrations reflects a characteristic feature of recently regenerated volcanic soils [54].
Carbon concentrations (0.52–3.18%) fell within the range established for soil quality by [55]. Soil carbon plays a fundamental role in maintaining ecosystem functions, representing nearly twice the carbon stored in vegetation and the atmosphere combined [59,60].

3.3. Physical Parameters of the Forage

The study evaluated two forage species commonly cultivated in the area for cattle grazing: English ryegrass (Lolium perenne) and Kikuyu grass (Pennisetum clandestinum). The results of the physical analyses are presented in Table S4. Forage pH values (5.76–6.25) were below the optimal value of 6.4, indicating a slightly acidic condition that increases susceptibility to insect attacks, disease, and nutrient deficiencies in Ca, Mg, K, Na, and P, all of which are essential for plant development. Electrical conductivity values were considerably higher in forage than in soils (3.13–8.29 µS/cm) (Table S4), suggesting a high capacity for salt absorption. Sodium, in particular, tends to accumulate in aerial parts, where it disrupts metabolic processes, reduces chlorophyll content, and inhibits growth [61].
Organic matter content in forage was high (84.12–90.19%), composed mainly of C, H, N, and O, which together account for 90–95% of the plant dry matter [58]. These results reflect the typical composition of grasses in volcanic regions, where acidic conditions and salt uptake influence plant nutritional quality.

3.4. Macronutrients in Forage

The results of the macronutrient analysis for forage are presented in Table S5. Potassium levels (7666.50–16,916.50 mg/kg) were within the reference range for plant nutritional requirements (10,000–50,000 mg/kg) [58]. Potassium deficiency can cause plant wilting, leaf necrosis, chlorosis, and greater root susceptibility to disease. In contrast, sodium concentrations (17,396.00–415,018.91 mg/kg) were considerably higher than the optimal requirement of 10 mg/kg established by [58], suggesting a risk of phytotoxicity. Excess Na often reduces K uptake and leads to shortened roots and stems, fewer leaves, and impaired plant growth.
Phosphorus concentrations (70.80–148.60 mg/kg) were well below the recommended threshold of 2000 mg/kg [58]. Phosphorus deficiency is typically expressed through dark green leaf pigmentation, stunted growth (dwarfism), and delayed maturity, given the element’s essential role in metabolism and development [62]. Comparative studies by [63] on similar forage species reported higher concentrations of K, Na, and P than those observed here. During sample collection, visible nutrient stress symptoms were noted, likely linked to these imbalances.
Nitrogen concentrations ranged from 1.00 to 3.63%, with half of the samples falling within the optimal range of 2–5% [64], while the remainder showed suboptimal values, indicating possible nitrogen deficiency due to limited N mineralization under local environmental conditions (soil moisture, temperature, and pH). Carbon concentrations (31.03–58.66%) were largely consistent with the adequate range defined by [65], which identifies 42% as optimal, and were higher than values reported by [66] (29.14–30.86%) in the aerial parts of high Andean native grasses.

3.5. Physicochemical Parameters of Milk

The results of the physicochemical analyses of raw milk samples are presented in Table S6. pH values ranged from 6.66 to 6.92. Samples M-01, M-05, M-11, and M-13 exceeded the acceptable range of 6.6–6.8 set by INEN 1500 and AGROCALIDAD, and only M-10 and M-12 met the more restrictive range of 6.5–6.7 proposed by [67]. Since pH reflects the concentration of free H+ ions in milk [68], elevated values may indicate mastitis, while lower values can suggest colostrum or microbiological contamination [67]. Relative density ranged from 1.0263 to 1.0330 g/cm3 (at 20 °C), with most samples within the 1.028–1.032 g/cm3 range of INEN 9:2012. Deviations in M-02, M-10 (low values), and M-14, M-15 (high values) were linked to variations in fat, solids-not-fat (SNF), and sample handling [69]. Fat content in M-14, M-15, and M-16 fell below the 3% minimum of INEN 9:2012 but remained within the broader 2.2–8% range of [67]; fat is essential for transporting fat-soluble vitamins and providing bioavailable lipids [70].
Total solids (TS) ranged from 11.58 to 14.54%, exceeding the 11.2% minimum of INEN 9:2012 in all samples, with most surpassing the 12% threshold of [67]. Protein ranged from 3.03% to 3.48%, above the INEN minimum (2.9%) and within the 2.7–4.8% range reported by [67]. Milk proteins include caseins, α-lactalbumin, β-lactoglobulin, serum albumin, immunoglobulins, enzymes, and non-protein nitrogen fractions. All samples (8.25–9.51%) also met the 8.2% minimum for SNF established by INEN 9:2012, reflecting contributions from proteins, lactose, and minerals. Lactose levels (4.57–5.30%) were generally within the 4–5% range [71], but six samples exceeded this threshold, with M-13 reaching 9.51%, which is even higher than the 3.5–6% range reported in [67].
Freezing point values were consistent with standards and showed no evidence of adulteration with water, falling within −0.61 °C to −0.52 °C (INEN 9:2012), and the −0.61 °C to −0.50 °C range suggested by [67]; all results were well below 0 °C, the freezing point of pure water [72]. Mineral salt content (0.68–0.78%) generally fell within the 0.65–0.90% range of [67], with salts composed primarily of Ca, P, Mg, K, Cl, S, citrates, and carbonates, alongside trace elements such as Fe, Cu, Al, Zn, Mn, Co, Ni, Pb, As, Cr, Se, F, and Br. Electrical conductivity values (3.59–5.86 S/m) also aligned with the reference range of 4.0–5.0 S/m [73], confirming overall compliance with accepted compositional standards.

3.6. Metal Analysis

3.6.1. Soils

Descriptive statistics showed that the median concentrations of Pb (1.572 mg/kg), Cd (0.329 mg/kg), and As (1.349 mg/kg) in the soil samples were below the reference limits established by Ecuadorian regulations [74], namely 19 mg/kg for Pb, 0.5 mg/kg for Cd, and 12 mg/kg for As. In contrast, Hg (1.818 mg/kg) and Se (1.345 mg/kg) exceeded their respective thresholds of 0.1 mg/kg and 1 mg/kg, as detailed in Table S7. Correlation analysis (Figure 1) revealed strong associations between heavy metals and soil physicochemical parameters. A strong correlation between Hg–OM (r = 0.80) and Hg–C (r = 0.75) suggests that Hg interacts closely with organic matter, binding with reduced sulfur sites and organic compounds, which enhances its solubility, mobility, and toxicity [75,76]. Similarly, Se–C correlations (r = 0.62) highlight the role of organic matter in Se retention and mobility [77].
Interactions among heavy metals were also evident. A positive Se–Hg correlation (r = 0.62) supports evidence that Se can reduce Hg bioaccessibility and bioaccumulation in plants, likely through insoluble Hg–Se complexes in the rhizosphere or roots, or via geochemical association as selenides [78,79]. Likewise, Se–Cd correlations (r = 0.62) suggest Se may transform Cd into less mobile fractions through complexation or coprecipitation, depending on whether it occurs as selenite (SeO32−) or selenate (SeO42−) [80,81]. Cd also influences Se mobility via adsorption–desorption dynamics on iron and manganese oxides.
Negative correlations indicated further soil–metal interactions. Pb–N (r = −0.69) implies that Pb reduces nitrogen availability, potentially impairing plant growth and biomass production [22,82], while Pb–pH (r = −0.57) reflects enhanced Pb solubility under acidic conditions [83]. Selenium also inhibits the uptake of several heavy metals (Hg, Cr, Cd, Pb, As) by plants, particularly in acidic and neutral soils (pH < 5.5), where it interferes with absorption pathways or forms stable complexes [84]. Additional moderate negative correlations were observed between Se–K (r = −0.53), Pb–real density (r = −0.54), Cd–real density (r = −0.55), and Cd–pH (r = −0.53), suggesting that soil properties strongly regulate the mobility and bioavailability of these elements.

3.6.2. Forage

The median concentrations of Pb (1.246 mg/kg), Cd (0.403 mg/kg), Hg (1.881 mg/kg), As (0.782 mg/kg), and Se (1.228 mg/kg) in forage and root samples are presented in Table S7. All values exceeded the reference limits for vegetables established by [85]—0.1 mg/kg for Pb, Cd, and Hg; 0.02 mg/kg for As; and 0.01 mg/kg for Se—based on water quality criteria [86]. Nevertheless, As, Cd, and Pb concentrations fell within typical ranges reported for plants by [87], whereas Hg levels were substantially higher, indicating significant bioaccumulation in plant tissues.
The toxic effects of these elements on plants are well documented. Cadmium impairs plasma membrane permeability, reducing water content and ATPase activity in root plasma membranes [88], and disrupts chloroplast metabolism by inhibiting chlorophyll biosynthesis and CO2 fixation [89]. Mercury mobility and uptake are regulated by cation exchange capacity, soil pH, aeration, and plant species [90], though it often binds to clay and OM in soils. Lead is generally retained in roots, where it interferes with physiological processes, inhibits germination, reduces photosynthesis and growth [91], and induces morphological abnormalities [92]. Arsenic also shows phytotoxicity: in tomato, it reduces fruit yield and biomass [93]; in canola, it causes chlorosis, wilting, and growth inhibition [94]; and in rice, it limits germination, seedling height, leaf area, and dry matter production [95,96].
Correlation analysis (Figure 2) revealed several significant relationships between heavy metal concentrations and forage physicochemical parameters. A positive correlation was observed between Cd and electrical conductivity (r = 0.61), while negative correlations included Hg–P (r = −0.58), Se–N (r = −0.56), Cd–OM (r = −0.55), and Pb–P (r = −0.51). These associations highlight the influence of soil and plant chemistry on heavy metal mobility and accumulation.

3.6.3. Milk

The concentrations of Pb and Cd in milk samples were below the detection limits of the analytical equipment (0.01 mg/kg for Pb and 0.2 mg/kg for Cd). Pb values fall within the acceptable limit of 0.02 mg/kg [38], indicating no detectable contamination, although conclusions regarding Cd remain uncertain due to its higher detection threshold. Mercury was detected in 8 of the 16 milk samples, with two exceeding the general food limit of 0.01 mg/kg [97]. Typical background concentrations reported by [67]—0.010 mg/L Pb, 0.003 mg/L Cd, and 0.006 mg/L Hg—suggest that Hg in this study was elevated. Pb and Hg are strongly bound to soil particles, limiting mobility and transfer through plants, but direct soil ingestion by cattle may still represent a risk pathway [98]. Arsenic (0.83 mg/kg) was detected in three samples, two of which surpassed the Codex food safety limit of 0.01 mg/kg [97] and the 0.01 mg/kg threshold for drinking water [99].
Among the trace elements studied, As, Cd, and Se pose the greatest risk of entering the food chain and can endanger human and animal health even at subphytotoxic concentrations [98]. Correlation analysis (Figure 3) revealed several significant relationships in milk: a strong negative correlation between EC and Hg (r = −0.83), and moderate correlations between Hg and Se (r = 0.60), Hg and TS (r = −0.52), Hg and Se in roots (r = −0.61), and between fat content and Se in roots (r = −0.58). These associations suggest interactions between mineral composition, plant uptake, and milk quality.
Given the consistently high levels of Se across soil, forage, and milk, further analyses are presented in Figure 4. In soil, Se correlated positively with C (r = 0.62) and negatively with K (r = −0.54); in forage, it was negatively correlated with N (r = −0.56); and in milk, Se correlated positively with Hg (r = 0.60) and pH (r = 0.54). However, as shown in Figure 5, no significant cross-matrix correlations were observed for As, Pb, Hg, Cd, or Se, suggesting that plant uptake is influenced more by speciation, soil properties, and species-specific mechanisms than by total soil metal concentrations, highlighting the need for further research using causal approaches to better understand uptake and transfer processes.

3.6.4. Bioaccumulation and Biotransfer Factors of Heavy Metals

Descriptive statistics were used to calculate four accumulation and transfer factors (Table S8). The root bioaccumulation factor (BCF) showed values > 1 for Pb, Cd, and Hg, indicating significant accumulation in the roots. Mercury exhibited particularly high BCF values (up to 376.33), identifying the sampled species as strong Hg hyperaccumulators, followed by Cd and Pb. In contrast, As and Se showed BCF < 1, suggesting limited accumulation in roots. Stem bioaccumulation factor (BAF) values revealed higher accumulation in aerial tissues for Hg (2.10), followed by Cd (1.53) and Pb (1.40), while As and Se again showed values < 1, confirming their exclusion from aboveground tissues.
The translocation factor (TF) indicated efficient root-to-shoot transport for Se (1.53), Pb (1.34), and Cd (1.08), whereas Hg and As exhibited TF < 1, suggesting preferential retention in roots. These patterns are consistent with earlier reports [98], highlighting the differential mobility of metals within plants. Biotransfer factors (BTF) for Pb, Cd, and Hg could not be calculated because their concentrations in milk were below the detection limit. For As and Se, BTF values were <1, indicating minimal transfer from forage to milk and suggesting limited food chain risk through dairy consumption.
Finally, according to the Ecuadorian Technical Standard [38], the maximum permissible Pb concentration in milk is 0.02 mg/kg. In this study, Pb levels were not only below this limit but also below detection thresholds, confirming that Pb in milk poses no regulatory concern.

3.7. Limitations of the Study

This study has several limitations that should be acknowledged. First, the detection limits of the analytical equipment may have hindered the identification of low-level heavy metal concentrations, particularly in milk, thereby restricting the calculation of biotransfer factors. Second, the relatively small sample size reduces statistical power and limits the generalizability of the findings. Third, sampling was carried out at a single time point, which does not capture seasonal or temporal variations in metal concentrations. Finally, although a detailed description is provided, this exploratory study is based on correlation analyses, which restricts its ability to establish causation.
In addition, the study did not quantify actual human exposure or evaluate potential health risks, nor did it include metal speciation analysis—an important factor for understanding bioavailability and toxicity. These constraints underscore the need for future research employing more sensitive instrumentation, larger sample sizes, and longitudinal designs. Nevertheless, despite these limitations, this study offers one of the first integrated assessments of heavy metal transfer along the soil–plant–animal–milk pathway in a volcanic-impacted region of the Ecuadorian Andes, providing valuable baseline evidence for environmental health monitoring.

4. Conclusions

This study assessed the transfer of Pb, Cd, Hg, As, and Se along the soil–plant–animal–milk pathway in a volcanic-affected area of the Ecuadorian Andes. Elevated concentrations of these elements were found in soil and forage samples, exceeding WHO and national reference values in several cases. In contrast, raw milk samples generally showed low contamination: Pb and Cd were below detection limits, Hg and As exceeded food safety thresholds in only two samples each, and Se surpassed drinking water limits in most. Bioconcentration and translocation factors revealed accumulation of Pb, Cd, and Hg in plant roots and stems, effective Se mobility to aerial parts, and limited uptake of As. Biotransfer factors for As and Se were below 1, and Pb, Cd, and Hg were undetectable in milk, suggesting minimal transfer through the food chain. Overall, these results indicate that, despite contamination in soil and forage, locally produced milk presents a low immediate food safety risk to consumers. However, the high levels of contamination detected in forage represent a potential long-term hazard for animal health and, indirectly, human health through cumulative exposure. These findings highlight the need for regular monitoring programs, soil management and remediation strategies, and tailored guidance for livestock farmers to minimize heavy metal uptake in forage and ensure sustainable production. Beyond providing the first integrated assessment of heavy metal movement across environmental and biological matrices in this volcanic context, this study establishes a critical baseline that can inform risk management policies and practical interventions in similar high-risk regions.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture15192072/s1. Figure S1: Community Surveys during Clean-Up Events in Bilbao Parish. Figure S2: Map showing the georeferenced soil sampling locations in Bilbao parish. Table S1: Environmental conditions and georeferencing of the study area. Table S2: Physicochemical parameters in soil samples. Table S3: Soil macronutrients. Table S4: Physical parameters of the forage. Table S5: Macronutrients in forage. Table S6: Physicochemical parameters of milk. Table S7: Metals analysis in soil, feed, and milk. Table S8: Bioaccumulation and biotransfer factors of metals (BCF, BAF, TF, and BTF).

Author Contributions

L.C.-B.: Writing—original draft, Visualization, Formal analysis, Conceptualization, Methodology, Validation, Investigation, Data Curation. I.G.-T.: Writing—Review and Editing, Conceptualization, Methodology, Validation, Resources, Supervision, Funding acquisition. V.H.V.-O.: Writing—Review and Editing, Conceptualization. S.R.-R.: Writing—Review and Editing, Conceptualization. C.P.: Writing—Review and Editing, Conceptualization. Á.A.C.-B.: Writing—Review and Editing, Conceptualization. A.J.S.-P.: Writing—Review and Editing, Conceptualization, Validation, Formal analysis, Data Curation, Visualization, Supervision. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Higher Polytechnic School of Chimborazo (Ecuador), in the framework of the 226.CP.2020 project. Antonio J. Signes-Pastor is funded by CIDEGENT/2020/050—ESGENT/003/2024. Funding for some of the analyses was also provided by the project CIAICO/2023/198 financed by the Autonomous Community (Comunidad Valenciana) through Conselleria de Educación, Cultura, Universidades y Empleo.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data and original contributions presented in this study are included in the article. Any additional information beyond that presented in the article is available upon request from the corresponding author.

Acknowledgments

This study is part of the research project entitled: “Evaluation of the bioavailability of heavy metals and their degree of impact in the areas influenced by the Tungurahua volcano and a study of bioaccumulation in soils and products derived from agricultural activities”, carried out between the Associated Research Group in Biotechnology, Environment and Chemistry (GAIBAQ) of the Higher Polytechnic School of Chimborazo and the Environmental Research Group of Agrochemistry and Environment (GIAAMA) of the Miguel Hernández University of Elche, for which the authors appreciate their financial support and scientific contribution.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
PbLead
CdCadmium
HgMercury
AsArsenic
SeSelenium
PPhosphorus
NNitrogen
BCFRoot bioconcentration factor
TFTranslocation factor
BTFBiotransfer factor of heavy metals from forage to milk
ECElectrical conductivity
OMOrganic matter
TSTotal solids
SNFSolids not fat
SFNSolids not fat content in milk
LODLimit of detection
BAFAerial part bioaccumulation factor
pHHydrogen potential
DRReal density (for soil)
RDReal density (for soil)
KPotassium
CCarbon
HHydrogen
NaSodium
DcorrCorrected milk density
FPFreezing point (of milk)
SaltsMineral content (in milk)
INENEcuadorian Institute for Standardization
MAEMinistry of the Environment of Ecuador
Se_rootSelenium concentration in roots

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Figure 1. Spearman correlation analysis between soil physicochemical parameters and metal analysis. Element symbols: Se (selenium), Pb (lead), Hg (mercury), Cd (cadmium); other variables: pH (hydrogen potential), EC (electrical conductivity), OM (organic matter), DR (real density), P (phosphorus), K (potassium), N (nitrogen), C (carbon), H (hydrogen). All chemical concentrations are expressed in ppm (mg/kg). Positive correlations are shown in shades of blue, no correlation is shown in white, and negative correlations are shown in brown, as indicated by the color scale.
Figure 1. Spearman correlation analysis between soil physicochemical parameters and metal analysis. Element symbols: Se (selenium), Pb (lead), Hg (mercury), Cd (cadmium); other variables: pH (hydrogen potential), EC (electrical conductivity), OM (organic matter), DR (real density), P (phosphorus), K (potassium), N (nitrogen), C (carbon), H (hydrogen). All chemical concentrations are expressed in ppm (mg/kg). Positive correlations are shown in shades of blue, no correlation is shown in white, and negative correlations are shown in brown, as indicated by the color scale.
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Figure 2. Spearman correlation analysis between physicochemical parameters and metals analysis in forage. Element symbols: Se (selenium), Pb (lead), Hg (mercury), Cd (cadmium); other variables: pH (hydrogen potential), EC (electrical conductivity), OM (organic matter), K (potassium), Na (sodium), P (phosphorus), N (nitrogen), C (carbon), H (hydrogen). All chemical concentrations are expressed in ppm (mg/kg). Positive correlations are shown in shades of blue, no correlation is shown in white, and negative correlations are shown in brown, as indicated by the color scale.
Figure 2. Spearman correlation analysis between physicochemical parameters and metals analysis in forage. Element symbols: Se (selenium), Pb (lead), Hg (mercury), Cd (cadmium); other variables: pH (hydrogen potential), EC (electrical conductivity), OM (organic matter), K (potassium), Na (sodium), P (phosphorus), N (nitrogen), C (carbon), H (hydrogen). All chemical concentrations are expressed in ppm (mg/kg). Positive correlations are shown in shades of blue, no correlation is shown in white, and negative correlations are shown in brown, as indicated by the color scale.
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Figure 3. Spearman correlation analysis between physicochemical parameters and metals analysis in milk samples. Variable definitions: Se (selenium), Hg (mercury), Se_root (selenium concentration in roots), pH (hydrogen potential), density (milk density), fat (milk fat content), TS (total solids), protein (protein content), SNF (solids not fat), lactose (lactose content), FP (freezing point), salt (mineral content), and EC (electrical conductivity). Heavy metal concentrations are expressed in ppm (mg/kg). Positive correlations are shown in shades of blue, no correlation is shown in white, and negative correlations are shown in brown, as indicated by the color scale.
Figure 3. Spearman correlation analysis between physicochemical parameters and metals analysis in milk samples. Variable definitions: Se (selenium), Hg (mercury), Se_root (selenium concentration in roots), pH (hydrogen potential), density (milk density), fat (milk fat content), TS (total solids), protein (protein content), SNF (solids not fat), lactose (lactose content), FP (freezing point), salt (mineral content), and EC (electrical conductivity). Heavy metal concentrations are expressed in ppm (mg/kg). Positive correlations are shown in shades of blue, no correlation is shown in white, and negative correlations are shown in brown, as indicated by the color scale.
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Figure 4. Spearman correlation analysis of Se concentrations in soil, forage, and milk samples. Variable definitions: Se (selenium), Hg (mercury), Se_root (selenium concentration in roots), pH (hydrogen potential), EC (electrical conductivity), OM (organic matter), RD (real density), P (phosphorus), K (potassium), N (nitrogen), C (carbon), H (hydrogen), Na (sodium), density (milk density), fat (milk fat content), TS (total solids), protein (protein content), SNF (solids not fat), lactose (lactose content), FP (freezing point), and salt (mineral content in milk). Element concentrations are reported in ppm (mg/kg). Positive correlations are shown in shades of blue, no correlation is shown in white, and negative correlations are shown in brown, as indicated by the color scale. Panels: (A) Se in Soil; (B) Se in Forage; (C) Se in Milk.
Figure 4. Spearman correlation analysis of Se concentrations in soil, forage, and milk samples. Variable definitions: Se (selenium), Hg (mercury), Se_root (selenium concentration in roots), pH (hydrogen potential), EC (electrical conductivity), OM (organic matter), RD (real density), P (phosphorus), K (potassium), N (nitrogen), C (carbon), H (hydrogen), Na (sodium), density (milk density), fat (milk fat content), TS (total solids), protein (protein content), SNF (solids not fat), lactose (lactose content), FP (freezing point), and salt (mineral content in milk). Element concentrations are reported in ppm (mg/kg). Positive correlations are shown in shades of blue, no correlation is shown in white, and negative correlations are shown in brown, as indicated by the color scale. Panels: (A) Se in Soil; (B) Se in Forage; (C) Se in Milk.
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Figure 5. Spearman correlation analysis of heavy metals (As, Pb, Hg, Cd, and Se) in soil, root, and forage samples. Element abbreviations: As (arsenic), Pb (lead), Hg (mercury), Cd (cadmium), Se (selenium). Positive correlations are shown in shades of blue, no correlation is shown in white, and negative correlations are shown in brown, as indicated by the color scale. Panels: (A) As, (B) Pb, (C) Hg, (D) Cd, and (E) Se.
Figure 5. Spearman correlation analysis of heavy metals (As, Pb, Hg, Cd, and Se) in soil, root, and forage samples. Element abbreviations: As (arsenic), Pb (lead), Hg (mercury), Cd (cadmium), Se (selenium). Positive correlations are shown in shades of blue, no correlation is shown in white, and negative correlations are shown in brown, as indicated by the color scale. Panels: (A) As, (B) Pb, (C) Hg, (D) Cd, and (E) Se.
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Carrera-Beltrán, L.; Gavilanes-Terán, I.; Valverde-Orozco, V.H.; Ramos-Romero, S.; Paredes, C.; Carbonell-Barrachina, Á.A.; Signes-Pastor, A.J. Assessment of Heavy Metal Transfer from Soil to Forage and Milk in the Tungurahua Volcano Area, Ecuador. Agriculture 2025, 15, 2072. https://doi.org/10.3390/agriculture15192072

AMA Style

Carrera-Beltrán L, Gavilanes-Terán I, Valverde-Orozco VH, Ramos-Romero S, Paredes C, Carbonell-Barrachina ÁA, Signes-Pastor AJ. Assessment of Heavy Metal Transfer from Soil to Forage and Milk in the Tungurahua Volcano Area, Ecuador. Agriculture. 2025; 15(19):2072. https://doi.org/10.3390/agriculture15192072

Chicago/Turabian Style

Carrera-Beltrán, Lourdes, Irene Gavilanes-Terán, Víctor Hugo Valverde-Orozco, Steven Ramos-Romero, Concepción Paredes, Ángel A. Carbonell-Barrachina, and Antonio J. Signes-Pastor. 2025. "Assessment of Heavy Metal Transfer from Soil to Forage and Milk in the Tungurahua Volcano Area, Ecuador" Agriculture 15, no. 19: 2072. https://doi.org/10.3390/agriculture15192072

APA Style

Carrera-Beltrán, L., Gavilanes-Terán, I., Valverde-Orozco, V. H., Ramos-Romero, S., Paredes, C., Carbonell-Barrachina, Á. A., & Signes-Pastor, A. J. (2025). Assessment of Heavy Metal Transfer from Soil to Forage and Milk in the Tungurahua Volcano Area, Ecuador. Agriculture, 15(19), 2072. https://doi.org/10.3390/agriculture15192072

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