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As highly relevant environmental contaminants, metals and metalloids have been extensively evaluated for decades in biomonitoring programs, due to their potential toxicity at low levels and high persistence in many ecosystems. When considering chemical analysis, metal quantification has been carried out through conventional methods, based on the determination of their levels in internal organs, such as the liver and kidneys. Nevertheless, non-invasive methods constitute an alternative response regarding trace elements biomonitoring studies. Specifically, keratinized tissue from terrestrial mammals (such as hair, nails, or spines) presents a high accumulation rate, giving relevant information about heavy metal dynamics at internal levels and, most particularly, a chronic exposure. This critical review focuses on the use of non-invasive tissues, mainly hair and spines, as adequate tools on heavy metals assessment, specifically mercury (Hg) and lead (Pb), in biomonitoring studies performed in terrestrial wild mammals.
Toxicology Area, Faculty of Veterinary Medicine (UEX), Caceres, Spain
Marcos Pérez-López
Toxicology Area, Faculty of Veterinary Medicine (UEX), Caceres, Spain
Francisco Soler
Toxicology Area, Faculty of Veterinary Medicine (UEX), Caceres, Spain
María Prado Míguez-Santiyán
Toxicology Area, Faculty of Veterinary Medicine (UEX), Caceres, Spain
Salomé Martínez-Morcillo*
Toxicology Area, Faculty of Veterinary Medicine (UEX), Caceres, Spain
*Address all correspondence to: martinezmorcillo@unex.es
1. Introduction
1.1 Wild terrestrial mammals as sentinel species
The presence of a broad spectrum of contaminants in the environment has led to the need to seek methods for the early detection of environmental disturbances that endanger biodiversity. One of the most relevant pollutants is inorganic elements such as heavy metals, and according to Ali & Khan [1], “Heavy metals are naturally occurring metals having atomic number greater than 20 and an elemental density greater than 5 g cm−3.” Their potential toxic effects at low concentrations and high persistence in the environment give them importance from a toxicological perspective. Systematic measurements of physical or chemical parameters carried out in the abiotic environment (water, air, soil, or sediment) are not enough, as they do not provide information and do not guarantee the representativeness of the data as far as the concentrations of toxicants in wildlife are concerned.
Over the past decades, the use of biomonitoring species has been established as a methodology for the determination of inorganic and organic contaminants. Biomonitoring includes bioindicator organisms, whose presence/abundance or absence provides a qualitative response on the availability of pollutants in the environment in which they develop. Besides, biomarkers are tools that consist of measuring biological responses of an organism exposed to any agent, providing in this case quantitative information [2]. In most of these programs, organisms from different taxonomic groups have been used, such as mammals, birds, and/or fish, whose physiological system is very complex, being potential bioindicators for metal pollution [3]. This is favored because these organisms have a high potential for accumulation and resistance to those, and a great sensitivity to environmental conditions, as well as constant weight and size, wide abundance and distribution, easily interpretable results, and can be extrapolated to the field of human health [1, 3, 4].
On terrestrial ecosystems, wild mammals are mainly chosen as potential sentinels of environmental pollutants loading because they are extremely linked to the environment [5]. Therefore, they are highly exposed to heavy metals through food intake, inhalation, and/or skin absorption, further contributed to by behavioral habits, such as grooming and burrowing, or physiological process, such as placental transfer during pregnancy [4]. In addition to the level of exposure on mammals, there are other intrinsic biological variables, which can influence metal uptake and retention in an individual, such as sex, age, species, tissue sampled, dietary habit, and season of sample collection [6]. Moreover, mammals are also commonly used in toxicological studies as experimental models to assess the risk of toxic exposure in humans [6, 7]. In general, the use of animals implies a number of advantages, which provides us temporal and spatial information on the presence of the pollutants. These animals are considered to be appropriate sentinel organisms since they can accumulate high levels of inorganic elements. Therefore, mammalian body burdens and responses are uniquely realistic indicators of mammalian exposure to chemicals [5].
1.2 The use of non-invasive tissues
Heavy metals are stored in different animal tissues at different rates and amounts. In most biomonitoring programs, the analysis and quantification of heavy metals in mammals are mainly performed in internal tissues, where they exert their main mechanism of action or bioaccumulate, such as liver, kidneys, brain, muscle, or bone [8, 9, 10, 11]. Liver and kidneys are more frequently analyzed because they have a high affinity for metals, and therefore, both reach the highest concentrations in the body [8, 10]. In addition, the use of internal tissues provides information on toxicokinetics, metal-specific organic lesions, or diagnosis. These organs reveal information about exposure to the toxicant in a short period of time (poisoning cases) but also can reflect long-term metal exposure to low doses [12]. However, the sample collection of these tissues requires the sacrifice of the animals, which can be due to various causes such as traffic accidents, diseases, hunting, poisoning, or trapping the animals and killing them for the study purpose [12, 13, 14, 15]. But it is evident that the sacrifice of the specimen carries strong ethical implication, even more so when focusing ecotoxicological studies on protected or endangered species. Faced with this situation, non-invasive methods constitute an alternative response to biomonitoring studies of inorganic elements.
A part of metal which is not subject to bioaccumulation in the internal organs is removed to a small extent through sweat, respiration, tears, or saliva [12, 16] and mainly through feces, urine, nails, feathers, hair, and spines [12, 17, 18, 19]. In the past decades, the use of these non-invasive samples has been approved as a helpful tool to monitor wildlife when compared to conventional methods because they do not induce pain or involve minimal stress for the individual, and as mentioned above, samples are taken without sacrificing the animal [12, 20, 21]. Moreover, the use of those matrix gives us some advantages; for examples, they are easy to obtain, transport, and store and allow successive measurements and assessing metal levels of the same individuals or population during a long period. For this reason, the use of non-invasive matrices is becoming increasingly important, especially when dealing with endangered, threatened, or sensitive species [20, 22].
1.3 Hair and spines
Hair samples have been shown to be promising for minimally invasive biomonitoring of global ecosystems pollution using sentinel species. This tissue provides relevant metal concentrations, resulting in the fact that it is able to incorporate and retain chemicals through the hair follicle, and constitute an elimination pathway from the body when it grows [20, 23, 24, 25, 26]. It is composed of keratin, protein rich in cysteine, whose structure is composed of sulfur and thiol (sulfhydryl, SH-) groups, and thus constituting a suitable matrix, which allows the affinity binding of metals such as Hg, Pb, Cd, or As [27]. Moreover, it is worth mentioning that hair contains up to 30% of cysteine [27, 28, 29]. This hard tissue, due to its chemical composition, is metabolically and biologically inactive. In addition, hair is an epidermal appendage that contains three layers. First, the medulla is the most internal layer composed of columns of keratinized cells and is covered by the cortex, which is the second layer composed of pigments, and at last, this structure is protected by the cuticle; this third layer consists of species-specific cell plates [30]. Therefore, these layers have affinities for different chemicals; the two internal layers are engaged in pigments that provide the properties to link metals; meanwhile, the external layer is made up of sulfur group and, as mentioned above, has a special affinity for bonding with metal [18, 30]. In this stance, the metal’s absorption ability could vary in relation to the hair morphology, differing among mammalian species [18, 27]. As a result of the fact that the hair, specifically the hair follicle, is in close contact with the bloodstream, it constitutes one of the major pathways for the excretion of metals that are incorporated into the matrix as it grows. Besides internal metal accumulation by blood, the external assimilation by the soil or air of metals that are continuously incorporated into the hair shaft during growth must be considered too [31, 32, 33]. It is noteworthy that according to the United Nations Environmental Program [34], hair is chosen as one of the most important materials for biological monitoring worldwide in the Global Environmental Monitoring System.
Spines are strong and durable structures, which play a defensive role [21, 35]. This kind of keratinized tissue is altered hair that has suffered a process of keratinization. Thus, it is expected to have a similar potential as hair in heavy metal assessment. These structures are composed of a porous core and dense shells. The solid columns evolve into a hollow for reducing weight or into a foam structure for preventing ellipticity. This kind of structure can develop in a longitudinal or transversal way [36]. Moreover, both are extremely in contact and may reflect long-term exposure to toxic metals because of their relatively slow rate of growth [37]. In this context, both inert matrices, hair and spines, are solid and durable in nature and are often used in ecotoxicological studies as alternative tools in order to minimize the employment of lethal techniques.
Hence, heavy metals are partly eliminated and sequestered by these keratinized tissues, but molting should be considered as a relevant factor on excretion pathways [38]. Some authors have observed that before molting, the hair contains higher amounts of metals than during, or just after molting [39, 40]. So molting could have a key role as an influencing factor on the metal accumulation in the hair.
This systematic review was performed in different databases including Web of Science, Scopus, and PubMed, and using different combinations of the following keywords: “biomonitoring,” “mammals,” “trace elements,” “heavy metals,” “mercury,” “lead,” “hair,” “spines.” All data were selected when literature on hair and spines as measurement tools for mercury and lead exposure was available.
In this review, 63 studies from 24 different countries have been reviewed. Mercury and lead have been quantified in 41 and 31 studies, respectively. Both metal data appear in 9 different studies. This review would be the first report that presents data on these heavy metals in hair and spines from 69 different terrestrial mammal species. Figure 1 shows the methodology and distribution of the studies reviewed.
Figure 1.
Summary of the methodology and distribution of the studies reviewed: Use of non-invasive tissues for biomonitoring of Hg and Pb in terrestrial ecosystems.
Table 1 compiles data regarding Hg levels in spines and hair of different mammal species. The average Hg concentration in the hair of terrestrial mammals is 40.91 ± 32.27 ppm from 0.022 to 2010 ppm. However, unique data of Hg on spines have been carried.
Concentration of mercury in hair and spine of small, medium, and large terrestrial wild mammals. Levels are expressed as mean (dry weight). Ranges are given when data were available.
Wet weight (ww).
n.d. (non-detected).
Considering a potential chronic exposure of terrestrial wild mammals, at low Hg concentrations via food, water, and ambient air, Hg toxicokinetic is well described [78, 79, 80]. Emphasizing on Hg excretion pathways, one of the most relevant is through the feces (85–90%) and to a lesser extent urine (5%) [79]. On the other hand, an appreciable Hg amount present in the blood stream is distributed and incorporated into the hair follicles [81, 82, 83]. Several studies have established that hair is another main route of excretion, even representing more than 80% of the total burden [78]. In the past decade, hair has been established as an elemental tool for biomonitoring studies concerning Hg in humans [84, 85, 86], associated with the fact that the composition of such keratinized matrices is suitable for Hg accumulation. Multiple studies have demonstrated the high affinity of Hg to hair, which can be reached during the growth period of the coat and bioaccumulate over time [18, 47]. The mercury-containing moiety binds to thiol groups in membrane proteins and enzymes, thereby interfering with the membrane structure and function, and with enzyme activity. This affinity is one of the main factors underlying the biochemical properties of Hg and its compounds. Some authors have observed under laboratory and field conditions that this hard tissue is able to accumulate environmentally relevant Hg residues in comparison with internal organs from mammals [45, 56, 87, 88]. It should also be considered that the biological half-life of Hg is higher in hair when compared to those. Therefore, levels of Hg in hair are a manifestation of chronic exposure [5]. Various studies have observed the hair as a good indicator of the Hg amount in the body, showing high correlation between metal concentrations in hair and internal organs, where biotransformation and bioaccumulation occur, such as liver, kidneys, or brain [52, 89, 90, 91, 92, 93]. Therefore, this allows us to conclude that hair represents a non-invasive approach for monitoring Hg accumulation in wild terrestrial mammals and the environment.
The only study carried out on spines that stands out, the one focused on the Brandt hedgehog (P. hypomelas) [35], determined that animals from agricultural areas had higher Hg concentrations in comparison with those from forest areas (31 and 23 ppb, respectively). These results proved strong evidence that spines can reflect the level of exposure to Hg in areas associated with human activities, such as the massive use of pesticides. Contrary to that indicated for spines, Hg concentrations in hair have been widely described for mammals. In small terrestrial mammals, Hg concentrations ranged from 20.1 ppb (P. Alecto) in unpolluted areas of eastern Australia [43] to 132 ppm (M. lucifugus) surrounding an industrial source with historical Hg contamination in North America [42]. Moreover, the last author reported the maximum value quantified in small mammals (274 ppm). In relation to medium-sized mammals, Hg concentration in hair ranged from 0.044 ppm (C. lupus in Italy) [27] to 2010.4 ppm (P. onca living in the gold mining area of Brazil) [59], this last value being the highest ever recorded in a wild animal. In large mammals, the range was between 0.022 ppm (Cervus elpahus in Austria) [70] and 0.34 ppm (R. tarandus platyrhynchus in Norway) [72]. However, the highest Hg concentration (0.532 ppm) was detected in a S. scrofa individuals from Russia [69]. These ranges would reflect that the degree of exposure depends on dietary habits [94], being lower in large mammals, whose dietary habits are mainly herbivorous, and higher in species, which occupy the medium and top of the food chain, whose species are mainly omnivores and carnivores [95]. Given the importance of the diet, some researchers have shown a strong association between dietary uptake and Hg accumulation in hair. It has been established that about 20% of Hg administered in the diet will end up in hair [96]. For example, Wang et al. [97] observed that Hg was mainly excreted and incorporated into the hair of mink after 60 days of feeding experiment, exposed to a total dose of 0.676 ppm MeHg chloride, and establishing a biomagnification factor (expressed as coefficient between hair and diet) of 69.1. In other similar experiments carried out in rats for 90 days with rice containing 51.3 ppb Hg, a major proportion of Hg was primarily bioaccumulated in kidneys and secondarily in hair, Hg being excreted through feces predominantly [98]. Moreover, in the studies by Wada et al. [48] and Yates et al. [99] carried out in different species of bats, a further insight into the tight correlation between endogenous levels in blood and transfer kinetics into the hair was observed, blood representing a dynamic balance between recent dietary exposure and tissue accumulation [100].
Aulerich et al. [14] fed minks a dose of 5 ppm of MeHg for a month and established a ratio of Hg burdens in hair, liver, kidneys, muscle, and brain for mustelids of 10:5:5:2:1. Although all minks died, this experiment reflects the short-term exposure to Hg and its acute effects on the organism, the liver and kidneys being the main target organs affected by this exposure, whereas hair had the lowest Hg level, surely due to the absence of hair growth during the experiment. These results suggest that Hg levels in hair are extremely linked to dietary exposure, this heavy metal being transferred and biomagnification through the trophic web.
Among other factors, age is considered to be a key factor, which can influence metal accumulation. As Hg has a low removal rate, its concentrations in hair are expected to increase with age as previous studies have reported [101]. Adults can be assumed to have bioaccumulated higher Hg concentration in hair when compared to juveniles because of their long-term exposure. Dahmardeh Behrooz et al. [35] observed that old European hedgehogs had high levels of Hg in spines (94 ppb) in comparison with juveniles (20 ppb) or pups (2 ppb); thereby a positive correlation between Hg levels in spines and age was observed. As widely described for other mammals, this observation has also been previously shown in the fur of bats [43, 99], mustelids [38, 56, 101], and other terrestrial wild mammals [58].
Similarly, sex should be another relevant factor to be considered when contemplating metal accumulation. However, a common pattern of Hg accumulation on keratinized tissues is not established. It has been observed how females can accumulate high Hg levels in hair in comparison with male terrestrial mammals [43, 47, 56, 89, 99, 102], while other authors have reported higher Hg concentration in hair and spines from male than females [35, 38]. These differences could be attributed to different factors, such as the foraging rate of female during the breeding season or their maternal transfer to the fetus during the gestation and lactation periods [29] as well as differences among dietary uptakes due to sexual size dimorphism (male preys on larger animals present in high levels of food chain) or some physiological differences (females are able to demethylate MeHg more efficiently than males and excretion rate) [103]. Indeed, the Hg bioavailability and toxicokinetics in terms of sex are not yet well understood due to the differences in hormonal and reproductive states, gene expression, and the metabolic rate between males and females [103]. In fact, the influence of sex on metal accumulation in hair has been investigated to a lesser extent, making it necessary to clarify the toxicokinetics of each inorganic element in males and females of different species and to consider this factor in future biomonitoring studies [104].
When focusing on hair, some researchers have concluded that the normal background level of Hg in the hair of terrestrial wild mammals ranges between 1 and 5 ppm [87]. It is known that Hg levels above 6 ppm in hair would be associated with subclinical neurological effects [105]. Thereby, a threshold of 10 ppm Hg in hair can be related to neurobehavioral disorders [106]. However, some interspecies differences are evident, and for example, neuronal effects have been described at 30 ppm in mustelids such as river otter or mink [78], this concentration being considered as the lowest observed adverse effect level (LOAEL) for terrestrial mammalian wildlife.
Lead has extensively been quantified in hair from a wide range of wild terrestrial mammals, as shown in Table 2, and the average including all terrestrial species is 4.06 ± 0.82 ppm between 0.19 and 34.20 ppm.
Concentration of lead in hair and spine of small, medium, and large terrestrial wild mammals. Levels are expressed as mean (dry weight). Ranges are given when data were available.
Wet weight (ww).
LD (limit of detection).
This inorganic element has high environmental relevance, being bioavailable and assimilated by terrestrial wildlife through food or water intake. Due to its potential health hazards, Pb has comprehensively been studied [80, 119, 120, 121, 122]. When considering the elimination route, it is mainly excreted through urine (67%) and feces (33%); however, small amounts are also excreted through the hair, spines, or nails [18, 21, 122]. It has been described that Pb may be bound to cysteine and has a certain affinity for sulfhydryl contained in keratin; hence, when it is distributed by blood, lead is incorporated into the hair follicle while growing, due to its continuous contact with the bloodstream [27]. The affinity between Pb and blood should be highlighted since this matrix is the main source of metals incorporated into the hair. A large part of Pb is bound to erythrocytes (95%) because of enzymes which make up these cells [25, 122]. The strong positive association between both keratinized tissues (hair and spine) and blood has been evidenced in some wild mammals at different trophic levels [37]. Likewise, it has also been observed that a significant linear relationship exists among both keratinized tissues and internal organs such as liver, kidney, brain, lungs, and gastrointestinal tract for Pb concentrations in wild terrestrial mammals [21, 22, 23, 73, 110]. When considering biomonitoring programs in human beings, hair has also been widely used in Pb quantification [122]. Despite the fact that hair has been considered as a suitable tool for measuring long-term Pb exposure in mammals in biomonitoring studies, bones are mainly chosen as the best tissue since they provide the best estimate of body burden. Nevertheless, bone collection requires the animal to be dead; therefore, it is discarded as a non-invasive technique.
In small mammals, mean Pb concentrations ranged from 0.34 ppm (M. myotis) to 34.2 ppm (P. pipistrellus) in Germany. The higher Pb level (973 ppm) in H. auropunctatus was quantified in a polluted area from Hawaii [107]. In medium-sized terrestrial mammals, Pb levels ranged from 0.19 ppm (C. lupus signatus from Italy) [27] to 2.95 ppm (Vombatus ursinus in a mining area from Australia) [114]. Mora et al. [49] quantified 150 ppm of Pb in hair of Felis pardalis from Texas (US), these authors suggesting that the animal was exposed through consumption of preys captured near busy roadsides. In large mammals, the variation between species was even larger, ranging from 0.401 ppm in U. arctos from Poland [76] to 13 ppm in Camelus sp. in polluted areas from Egypt [28]. The highest Pb level was determined in S. scrofa from Turkey (81.80 ppm) [118]. In spines, the average Pb concentration was 3.88 ± 1.95 ppm, and the range of Pb levels in E. europaeus was narrower in comparison with hair, ranging from 0.54 [13] to 7.3 ppm [37]. Moreover, in the last study, it was quantified that the highest Pb concentration (17.2 ppm) existed in the hedgehog population near the nonferrous metallurgic factory.
In addition to the quantity and bioavailability of Pb exposure, as shown in these ranges, the accumulation in hair and spines relied on ecological factors such as diet and endogenous factors such as species, size, behavior, or season [123]. Small mammals represent the medium stage of the trophic webs since they have multiple diet habits (insectivorous, omnivorous, and herbivorous). Further, their high metabolic rates increase their food intake, being highly exposed to metal [5]. In addition, their high exposure is due in part to the fact that they are closely linked to soil particles during their life cycle (i.e., grooming habits, storing food in their burrow, covering, or burrowing habits) and through the ingestion of soil and invertebrates, which tend to retain great amounts of metals, such as earthworms, slugs, earwigs, or beetles [31, 37, 124]. Therefore, small mammals are expected to have the highest Pb concentrations in hair and spine from exogenous source (i.e., particles covering the outer surface) or from endogenous source (i.e., Pb assimilated mainly by the diet and incorporated through the blood) [24, 31, 40].
Attending to a range of Pb concentrations in large mammals, they are exposed to a greater extent. This may be due in part to the fact that most of them are herbivores, ingesting mainly polluted plants by atmospheric particle deposition or taking up from the soil. It is noteworthy that some plants are able to accumulate even more than 1000 ppm, thus constituting a potential risk to mammals that feed on them, especially those living near areas where fertilizers and pesticides are used [121, 125]. Some researchers have shown under laboratory condition a positive linear increase of the Pb concentration in hair from animals fed with supplemental Pb. For example, these results were observed by Choi et al. [126] in pigs fed with 200 ppm Pb for 56 days. Even in field conditions, the effect of dietary habits on Pb accumulation in hair has also been observed [127]. Besides inhalation and grooming, animals can also ingest Pb from contaminated drinking water or even small amounts of soil, which may lead to unintentional ingestion of ammunition. Moreover, it is worth highlighting that most of the large mammal species are hunted, and when the animals are not killed, the bullets are accumulated in the body for a long time [128]. However, according to Gall et al. [125], Pb concentration in hair relies on its bioavailability in the environment, individual factors such as age, and its mobility in the organism.
Age is an intrinsic biological variable, which influences Pb retention in mammal hair, older animals being exposed to longer periods of time, having a higher concentration in comparison with young animals. Hence, a clear Pb accumulation in hair has been shown in terrestrial wild mammals such as C. lupus signatus [20]. However, most studies have not observed an age-related influence on Pb hair concentrations. Hernández-Moreno et al. [20] and Beernaert et al. [23] attributed it to the fact that in mammals most of the Pb (90%) is well stored in bone tissues with an age-related pattern. When considering the sex factor, studies have observed differences in Pb concentrations between females and males. For examples, in the hair of D. virginiana, higher concentrations in females when compared to males were observed [47]. This result was confirmed in A. sylvaticus [23], C. lupus signatus [112], and C. capreolus [25], too. However, although females tend to retain higher Pb concentrations in hair than males, little is known about the accumulation pattern according to sex. Differences between the accumulation or excretion process, physiology, bodily growth, and the presence of specific metabolizing enzymes or sexual hormones must be assumed in biomonitoring studies [129].
Limit thresholds for Pb in internal organs such as liver or kidney have been well established; for example, a critical renal value, which cause toxicosis in mammal, is defined in 15 ppm; meanwhile, in liver it is 5 ppm [130]. However, a wide range of Pb toxic levels in different mammal species has also been established for liver, kidney, brain, urine, and blood [121]. In the last matrix, a concentration above 5 μg dL−1 causes neurobehavioral deficits and neurotoxicity and death when reaching 80 μg dL−1. Thus, despite the toxic limit thresholds for Pb in wild mammal hair have not been well described yet, some authors have established in other keratinized tissues, such as feather, clinical sign of poisoning at a Pb concentration above 4 ppm [121]. It is noteworthy that in human, Pb background levels in hair have been established in 20–25 ppm; nevertheless, those levels have been established in 12–15 ppm by other authors [131].
In this critical review, mercury and lead concentrations in hair and spine from wild terrestrial mammals have been summarized, in an attempt to validate the use of these two non-invasive matrices for biomonitoring purpose. In this sense, diet habit plays a key role when considering Hg accumulation, being higher in animals occupying the medium and top of the food chain (i.e., carnivores and omnivores). With respect to Pb, its concentrations are usually higher in mammals linked to the soil fraction (i.e., insectivores and herbivores). Furthermore, the endogenous factor such as age must be considered when quantifying heavy metals because of its linear relationship between time of exposure and bioaccumulation. Besides, the influence of sex should be also studied as different metal bioaccumulation patterns in hair and spine according to this factor have been observed. With these considerations, hair and spines can be suitable non-invasive tissues reflecting the internal metal levels, thus constituting a good alternative in order to avoid the sacrifice of wild mammals and at the same time providing an effective early warning system of metal pollution.
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Written By
Javier García-Muñoz, Marcos Pérez-López, Francisco Soler, María Prado Míguez-Santiyán and Salomé Martínez-Morcillo
Submitted: 13 February 2023Reviewed: 20 February 2023Published: 25 March 2023
Open access peer-reviewed chapter
