Abstract
Civilian and military activities are sources of water and soil contamination by inorganic and organic contaminants caused by shooting practices, warfare, and/or mechanized military training. Lead poisoning and contaminant bioaccumulation due to spent shots or other related military contaminants have been widely studied for mammals, birds, and plants. Although there are different papers on the impact on earthworms, information on micro and mesofauna (i.e., collembola, nematodes, etc.) is still scarce. Here, we review the published data regarding the impact of civilian and military shooting activities, including war-impacted areas, focusing on soil organisms, from microbial communities to the ecotoxicological effects on terrestrial organisms. One hundred eleven studies were considered where earthworms and enchytraeids were widely studied, especially under ecotoxicological assays with Pb and energetic-related compounds from military explosives. There is a lack of information on soil organism groups, such as mites, ants, or gastropods, which play important roles in soil function. Data from combined exposures (e.g., PTEs + TNT and PTEs + PAHs) is scarce since several studies focused on a single contaminant, usually Pb, when combined contaminants would be more realistic. Ecotoxicological assays should also cover other understudied ammunition elements, such as Bi, Cu, or W.
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Introduction
Civilian shooting ranges and military areas, including warfare-impacted areas, are hotspots for the accumulation of inorganic contaminants (potentially toxic elements [PTEs] such as As, Cd, Cu, Hg, Mn, Pb, Sb, and Zn) by ammunition weathering. Different organic contaminants can also be found in these kinds of facilities, such as: i) polycyclic aromatic hydrocarbons (PAHs) derived from fuel oil spills (Price 1998; Bu-Olayan et al. 1998) or contained in the mobile clay targets on trap shooting ranges (Baer et al. 1995; Peddicord and LaKind 2000; Rodríguez-Seijo et al. 2017), ii) explosives derived compounds and propellants (Pichtel et al. 2012; Via and Zinnert 2016), iii) chemical warfare agents (CWAs) (Broomandi et al. 2023), or iv) polychlorinated biphenyls (PCBs) and per- and poly-fluoroalkyl substances (PFAs) (Skalny et al. 2021; Ruyle et al. 2023). Other activities, such as mechanized military training (e.g., infantry or tank training areas), can also harm soil properties through compaction and changes in nutrient cycles (DeBusk et al. 2005; Althoff et al. 2007; 2010). Bombs or heavy artillery can also impact soil properties due to the bombturbation process through landscape and soil structure changes (Hupy and Schaetzl 2006). Usually, these impacts will affect the belowground biota (Quist et al. 2003; Althoff et al. 2009).
Lead has been the most studied inorganic contaminant due to it being one of the main ammunition components (> 90% mass of bullets and shot pellets) (Sanderson et al. 2012; Reigosa-Alonso et al. 2021). The environmental impact of ammunition on soil and biota was ignored for decades, assuming that Pb from bullets remained inert in the metallic form as Pb0. When this Pb reach the soil system, it can be slowly weathered into more mobile forms (e.g., Pb2+ or Pb4+), which can quickly enter the food web via plants or soil organisms (Vantelon et al. 2005; Sanderson et al. 2012). This issue is not only related to Pb since civilian and military ammunition contain other elements (e.g., Bi, Cd, Cu, Sb, W, or Zn) that can be released into the environment and enter the food chain after ammunition weathering (Fayiga and Saha 2016; Rodríguez-Seijo et al. 2017; Sanderson et al. 2018; Barker et al. 2021). There is a similar issue for organic contaminants, such as PAHs from clay shooting ranges, energetic compounds from explosives and bombs, and CWAs from military areas (e.g., 2,4,6-trinitrotoluene (TNT), dinitrobenzene (DNB), nitroglycerine (NG), etc.). As reviewed by different authors (Baer et al. 1995; Robidoux et al. 2004a, b, c; Sarrazin et al. 2009; Certini et al. 2013; Broomandi et al. 2023), their products or degradation compounds can be easily taken up and bioaccumulated by soil biota.
In this sense, the use of Pb ammunition for military, civilian sport shooting, and hunting-related activities over the decades has released megatonnes of Pb that remain in the environment and are a persistent contaminant with adverse effects on wildlife. The Pb is neurotoxic to wildlife and humans (Sadiku and Rodríguez-Seijo 2022), and it has been widely studied in terrestrial vertebrates, such as mammals and birds, with > 1,000 papers published between 1953 and 2020 (Di Minin et al. 2021). They have a significant ecological and economic interest, but they are also highly exposed to these ammunitions through recreational hunting and/or due to direct uptake from the environment (Haig et al. 2014; Mateo et al. 2014; Williams et al. 2017; Di Minin et al. 2021). More than 240 European mammal species have been identified with a risk of exposure to Pb from ammunition and fishing weights. Each year in Europe, more than 1 million wildfowl are killed by Pb poisoning, and nearly 3 million individuals have suffered sub-lethal effects by lead ammunition ingestion (Pain et al. 2009, 2019; Di Minin et al. 2021; Chiverton et al. 2022). A similar question can be indicated for terrestrial plants since their distribution is usually limited by the high contents of contaminants in soils, although some native species from shooting areas can also be used for phytoremediation purposes, both for inorganic and organic contaminants (Sanderson et al. 2018; Dinake et al. 2021; Broomandi et al. 2023).
However, knowledge regarding the impact of civilian and military ammunition on terrestrial organisms (excluding mammals, birds, or plants) is scarce, sometimes due to difficulties accessing these facilities for field sampling assays or doing ecotoxicological tests under laboratory conditions. Besides, this question can also be indicated for other ammunition-related contaminants. Research has been widely focused on Pb or single-contamination exposures, but other ammunition-related contaminants such as Cu, Zn, TNT, and DNB or multiple contamination scenarios are scarce. This research aims to overview the scattered literature on areas impacted by civilian and military shooting activities and improve the knowledge about the impact of ammunition on non-avian and non-plant groups. This review includes the impact of mechanical disturbances caused by military training activities and impacts by inorganic (PTEs) and organic contaminants (PAHs, TNT, DNB, and NG, among others).
Data collection
This review was performed using original research papers, including book chapters, articles, and review papers published in peer-reviewed journals, and collected by searching relevant research databases (Web of Science, Google Scholar, and SCOPUS). The search was focused on civilian sport shooting and military-impacted areas, including warfare-impact zones. Multiple search inquiries were made using keyword combinations including: “shooting range,” “firing range,” “warfare,” “military area*,” “hunting,” “lead ammunition,” “*munition,” “explosive,” “ecotox,” “organic contamination,” “heavy metal,” “TNT,” “clay target,” “toxic elements,” “military explosives,” “tungsten,” “bismuth” “trace metal*,” “bacteria,” “land snail,” “gastropods,” “protozoa,” “*worm,” “arthropods,” “amphibians,” “collembola,” “acari,” “ants,” “microarthropods,” “biotest” and “*toxicology”. The Boolean truncation (“*”) was used to ensure all keyword variants were found and available for data search. The literature search was initially conducted in February 2021 and updated in May 2024. The selected studies were differentiated between research in which i) organisms are exposed to contaminated or uncontaminated soils and ii) organisms directly collected from the field. Ecotoxicological tests with terrestrial plants or soil elutriate with aquatic organisms (e.g., microtox, cladocera assays (e.g., Daphnia magna), or algal elutriate assays) were not considered. The impact of fishing weights was also reviewed, although not included since it was not the main objective. Each selected research should provide information about location, organism, contaminant levels (application mode or environmental values), and main assessed endpoints. A search in selected databases identified 295 articles, of which 111 were retained after eliminating duplicates, and that accomplished the criteria mentioned above.
Soil microorganisms
Thirty-three studies have been conducted on the impact on soil microorganisms, including soil bacteria, fungal communities, and the soil microbial community, with inorganic and organic contaminants (Table 1, 2, 3). In general, soil microbiota biodiversity through biomass, microbial decomposition, or soil enzymatic activities, such as dehydrogenase activity, are adversely impacted over time by high levels of PTEs, both for pseudo total and available contents (Lee et al. 2002; Rijk and Ekblad 2020) (Table 1).
Similar effects on microorganisms have been described with PAHs (Rijjk and Ekblad 2020), explosive-related compounds, such as Trinitrotoluene (TNT) and their degradation products, hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX), 1,3,5-trinitrobenzene (TNB) or N-methyl-N,2,4,6-tetranitroaniline (Tetryl) (Table 1) (Gong et al. 2001; Lee et al. 2002). Although differences were observed between field collection or enzymatic assessment under laboratory exposure, in general, enzymatic activities have been inhibited with increasing contaminant levels (i.e., Park et al. 2003; Baek et al. 2004; Kähkönen et al. 2008). Besides, mechanized military training disturbances can also be a source of soil degradation and impact soil microbial activity in different ways. Althoff et al. (2009) observed that microbial growth is immediately adversely impacted. However, over time, these populations can be increased due to the formation of new pores, and Gram-positive over Gram-negative bacteria can be favoured by this physical disturbance (Table 1). Nevertheless, the formation of these new pores as micropores and their impact on soil microorganisms are not fully understood.
Although soil fungal communities can grow under several soil types, a growth fungal reduction has been reported under higher Pb levels (Kähkönen et al. 2008), and soil microbial community composition can also be affected by the dominance of specific groups under Pb-contaminated soils (Hui et al. 2012; Sullivan et al. 2012) (Table 2). This question has also been highlighted by PLFA (Phospholipid-derived fatty acids) analysis, which provides information about the composition of large and important main microbial groups (Joergensen 2022). In this sense, soil microbial community composition can be impacted due to ammunition weathering (Rantalainen et al. 2006; Ringelberg et al. 2009; Selonen and Setälä, 2017), petroleum hydrocarbons or explosives degradation (Ringelberg et al. 2008; Mair et al. 2013) (Table 3). Besides, ammunition destruction sites are the most polluted areas in military sites. Some works have been carried out there and highlighted that different energetic compounds can migrate until 100 cm below the surface area (Zhang et al. 2023), and bacterial diversity and community composition are significantly impacted in these sites (Luo et al. 2023; Zhang et al. 2023). According to Zhang et al. (2023) and Luo et al. (2023), the microbial diversity in these areas is mainly controlled by pH, organic matter content and the different energetic compound residues (TNT, TNB, etc.).
However, some in-situ microorganisms can also be used for bioremediation purposes since they can be adapted to higher concentrations of contaminants (Hawari et al. 2000; Ringelberg et al. 2008; Mair et al. 2013), and for bioremediation purposes by indigenous soil microorganisms can be improved under NPK fertilization and at increased temperature (Siles and Margesin 2018) (Table 3). In this sense, tolerant microorganisms have been observed in the soil litter layers from high-contaminated soils by Pb (Hui et al. 2009, 2012), fuel spills (Mair et al. 2013; Siles and Margesin 2018) or explosives compounds (Isyaku and Otaiku 2019; Kim et al. 2024), while soil fungal communities can also bioaccumulate PTEs (Selonen et al. 2012), explosives comounds (i.e., Otaiku and Alhaji, 2020) or PAHs (García-Delgado et al. 2015) (Table 2), that can be used for environmental remediation.
Therefore, research is also needed on the isolation, identification and characterization of native populations (e.g., Pb-tolerant, TNT-tolerant, RDX- or NQ-degrading microorganisms, among others), which could help to understand soil microbiota and could be used for enhancing soil bioremediation capabilities.
Impacts on microfauna
Microfauna covers soil organisms with an essential role in the microbial diversity and functional stability, soil organic carbon cycle or availability of nutrients for plants, and sometimes with a role in the bioremediation of contaminated areas. Specifically, nematodes are the most abundant animal on the earth and a dominant component of microfauna in soil biota. Nematodes are widely used as bioindicators of soil quality due to their soil function as biocontrol agents, such as consuming disease-causing organisms. They have a high impact on soil fertility through the N mineralization into bioavailable forms for plants (Neher 2001; Chen et al. 2007; van den Hoogen et al. 2019). They are also excellent organismal models for different contaminants since they have a completely sequenced genome, rapid replication cycle, and easy culture conditions, among other reasons (Lu et al. 2020).
In the case of the impact of soil contamination by shooting and military activities, different studies have exposed nematodes to physical disturbances (Althoff et al. 2007, 2009), inorganic (Ellis et al. 2001; Lu et al. 2020) and organic contaminants (Kuperman et al. 2007; Gong et al. 2018; Ni et al. 2022) (Table 4).
In general, nematode communities are impacted by mechanized military training (Althoff et al. 2007, 2009) and organic contaminants (Gong et al. 2018; Ni et al. 2022), while nematode abundance and diversity showed diverse responses from significant reduction (Ellis et al. 2001; Kuperman et al. 2007) to no changes (Rantalainen et al. 2006) (Table 4). Rantalainen et al. (2006) suggested that nematodes are short-generation-time organisms and could develop a Pb tolerance over time when exposed to inorganic contaminants. However, this question does not seem similar for organic pollutants, as shown for mustard gas (Kuperman et al. 2007) or TNT (Ni et al. 2022), with significant effects on oxidative stress levels (Table 4).
Regarding protozoan studies, only two were found, with some differences according to the contaminant. Fuller and Manning (1998) reported that protozoa are negatively associated with high levels of TNT (up to 27,153 mg kg−1) and TNB (up to 305 mg kg−1). However, Selonen and Setälä (2015) did not find correlations between soil Pb (19,100–50,300 mg kg−1) and protozoan abundance. They only showed an impact on abundance under different soil pH values since soil pH is the main parameter regulating protozoan abundance (Xu et al. 2022). No studies were found with tardigrades or rotifers. In addition to laboratory studies, further studies should focus on field studies, with soil organisms extracted from contaminated field areas, to assess the potential lead tolerance over time on inhabitant organisms. In addition, combined contamination and its impact on microfauna organisms should also be evaluated.
Impacts on mesofauna
Enchytraeids
Enchytraeids are a worldwide mesofauna organism found in many soil types. Under some conditions, these organisms are less sensitive to environmental factors than earthworms, such as salinity or stress caused by organic contaminants (Amossé et al. 2018). They can substitute for earthworms when less abundant, such as in SOM mineralization and nutrient cycling roles (Pelosi et al. 2021). Despite this hypothetical low sensitivity to some stressors, different studies have demonstrated how abundance, growth and reproduction can be impacted by Pb contamination (Salminen et al. 2002; Rantalainen et al. 2006; Hui et al. 2009) and different kinds of explosive compounds, such as TNT, RDX, 1,3,5,7-tetranitro-1,3,5,7-tetrazocane (HMX) or hexanitrohexaazaisowurtzitane (China Lake compound 20, CL-20) (Dodard et al. 2003, 2005; Best et al. 2008) (Table 5). However, ammunition toxicity on enchytraeids can be modulated since i) they would usually be less toxic to organisms when the contaminant was recently added to the soil (Kuperman et al. 2003, 2005, 2006a, 2009), ii) they are more toxic in juveniles than adult stages (Dodard et al. 2003, 2005; Kuperman et al. 2006b), or iii) soil properties (e.g. soil pH level, CEC, Ca concentration and organic matter content) can mitigate the toxicity by Pb or TNT (Kuperman et al. 2013; Luo et al. 2014a; Zhang et al. 2019). Kuperman et al. (2013) reported that high levels of organic matter and clay-loam soils (but not sandy soils) might mitigate the toxicity of TNT and RDX for enchytraeids reproduction. In this sense, the organisms have water-permeable skin and prefer moist soils with medium to high organic matter contents and acid-to-neutral soil pH values, under which species diversity is increased (Jänsch et al. 2005). However, these conditions could be a risk for enchytraeids since Pb is more bioavailable under some conditions, such as acidity or soils that combine higher organic matter contents and acidity. In this sense, Pb bioaccumulation is linearly increased with increased total soil Pb levels, being pHCaCl2 the main factor for predicting Pb toxicity (Luo et al. 2014a; Zhang et al. 2019).
Microarthropods: Collembolans and mites
Microarthropods organisms are usually found in leaf litter and organic-rich soil layers. Together with earthworms, they have an essential role in soil structure, the mineralization of organic matter, nutrient cycling, and the biomass and activity of the microbial community due to their feeding activity. Migliorini et al. (2004, 2005) reported that contamination from shooting range areas did not significantly impact soil communities, although specific groups' abundance can be more frequent in shortfall areas (Migliorini et al. 2004; Bowman 2015). They can resist moderate PTE levels (up to 1898, 16.3, 76.9, 65, and 170 mg kg−1 of Pb, Sb, Ni, Cu, and Zn, respectively), being collembolan communities more tolerant to PTE levels than mites (Migliorini et al. 2004). Although some studies showed collembolans seem more sensitive to changes in soil properties than to contaminant levels (i.e., Domene et al. 2011; Joimel et al. 2022; Zhang et al. 2022), reported data showed that their soil preference (e.g. avoidance behaviour test), survival and reproduction endpoints can be highly impacted by contamination by different PTEs (Luo et al. 2014b; Gruss et al. 2019), TNT (Frische 2003) or mustard gas (Phillips et al. 2002) (Table 6). In this sense, tolerance and potential bioaccumulation are usually concentration-dependent, as reported for Pb (Selonen et al. 2012; Luo et al. 2015) or sulfur mustard (Kuperman et al. 2007).
Impact on macrofauna
Earthworms
Earthworms can be considered one of the most critical soil biota groups due to their role in the ecosystem as soil engineers through the formation of stable aggregates, improving bulk density and soil porosity, nitrogen mineralization, or organic matter decomposition (Vidal et al. 2023). Besides, they are excellent model organisms for ecotoxicological assays and are usually recommended by international guidelines since there is abundant knowledge about their ecology or behaviour against different toxins (OECD 2016).
This importance is reflected in 45 studies that cover the impact of ammunition, CWAs, or explosive compounds on these organisms (Table 7). As with other organisms, mechanized military training impacts earthworm abundance and diversity (Althoff et al. 2009). Although varied species have been studied (e.g., Diplocardia spp., Bimastos welchi, Aporrectodea trapezoides, A. rosea, Lumbricus terrestris or Eisenia rosea), 39 studies have been found with E. andrei and E. fetida (Table 7). In general, exposure to Pb is not always correlated with worm mortality in 28-day assays. Usually, worm mortality occurs on Pb levels over 2000 mg kg−1 (Luo et al. 2014c; Sujetovienė and Česynaitė 2019). However, growth and reproduction are usually significantly reduced, although sometimes dependent on soil properties (Luo et al. 2014c) or co-contaminants, such as other PTEs (Bi, Cd, Cr, Cu, Ni, Sb or Zn), HMX from explosive compounds (Berthelot et al. 2008) or PAHs derived from clay targets used for civilian shooting ranges (Rodríguez-Seijo et al. 2017) (Table 7).
The PTEs from ammunition impacted soils are usually taken up by worms under dose–response relationships (i.e., Hund-Rinke et al. 2005; Sneddon et al. 2009; Luo et al. 2014c; Rodríguez-Seijo et al. 2017; Česynaitė et al. 2021) (Table 7), since worms can uptake PTEs, but also inorganic and organic compounds through soil ingestion and dermal contact (Savard et al. 2010; Belden et al. 2011; Rodríguez-Seijo et al. 2017). Oxidative stress parameters such as enzyme activities (e.g., CAT, SOD, GST) and lipid peroxidation may significantly be affected in worms exposed to contaminated soils by ammunition weathering (Berthelot et al. 2008; Česynaitė et al. 2021). Other parameters, such as the lysosomal membrane stability, showed significant effects when exposed to Pb (Booth et al. 2003; Berthelot et al. 2008). Interestingly, Reid and Watson (2005) highlighted that field-collected worms could have a metal tolerance compared to exposed worms under artificially spiked soils. This question should be considered for comparative assays.
Although Pb is the main component of civilian and military ammunition, different understudied elements from civilian-military ammunition also need attention. Copper, bismuth, titanium, tungsten, or alloys such as steel, W–Ni-Co, or W-nylon alloys were proposed as alternative materials for lead-free ammunition both in civilian activities (e.g., game hunting) and military activities since they were indicated as non-toxic, less-toxic or inert elements (Jenkins 2015; Rodríguez-Seijo et al. 2016; Datta et al. 2017; Thomas 2019; Barker et al. 2021). Adverse effects on earthworms have been reported by W (Inouye et al. 2006; Felt et al. 2009; Strigul et al. 2009) or Bi (Omouri et al. 2017, 2018), although other works indicated that uptake is more dependent on soil properties (Felt et al. 2009; Bamford et al. 2011) (Table 7). Besides, tungsten ammunition bullets can be a source of other contaminants since tungsten ammunition can be made by a mixture of W with a high-density plastic polymer or nylon (around 95% W and 5% plastic polymer, respectively) (Felt et al. 2009; Thomas 2019; Barker et al. 2021). Therefore, the potential impact of other ammunition components, metal alloys, or plastic polymers, such as microplastics, should also be studied. Other elements, such as U and DU, widely used in military ammunition for projectile production and antitank penetrators (Handley-Sidhu et al. 2010; Skalny et al. 2021) also significantly affect cocoon production (reproduction endpoint), and that metal accumulation levels are usually concentration-dependent (Oliver et al. 2008; Stanley et al. 2014).
Organic contaminants, such as PAHs from clay targets (Rodríguez-Seijo et al. 2017), fuel–oil spills in military areas (Schaefer 2003), and/or explosive-related compounds (TNT, HMX, RDX, etc.) can have similar toxicity than PTEs to earthworms. However, not all contaminants behave the same way on worms. In the case of explosive-related compounds, such as TNT, seems to be a compound with significant adverse impacts on growth and reproduction (Robidoux et al. 2000, 2002; Schaefer 2004), concentration-dependent mortality (Robidoux et al. 1999, 2004c; Best et al. 2008) and is implicated in neurological disorders (Robidoux et al. 2004a, b, c, d; Gong et al. 2007). Also, TNT and RDX can be easily bioaccumulated and with a potential transfer to higher-trophic-level receptors (Sarrazin et al. 2009), although other contaminants such as 2,4-dinitroanisole (DNAN) can be bioaccumulated, being reduced over time in aged soils (Lotufo et al. 2016, 2021). In general, no effects on survival have been detected for HMX-contaminated soils, while a no clear tendency was observed for reproduction, with no effects (Kuperman et al. 2003) or significant reduction (Robidoux et al. 2001; 2002). As reported for enchytraeids, toxicity can be regulated similarly, usually being soil-property-dependent (Certini et al. 2013) and time-dependent for HMX, RDX, and DNAN (Simini et al. 2003; Lotufo et al. 2016, 2021). In this sense, soils with high clay and soil organic matter contents have a key role in adsorbing and inactivating TNT contaminants or reducing Pb and PAH bioavailability (Fuller et al. 2005; Rodríguez-Seijo et al. 2017). Interestingly, TNT decomposition products such as 2,4-dinitrotoluene (2,4-DNT), 4-amino-2,6-dinitrotoluene (4-ADNT), or 2-amino-4,6-dinitrotoluene (2-ADNT) can be more toxic than primary compounds (Lachance et al. 2004), while worm movement and activity on soil can favour the formation of the secondary compounds due to increased aeration (Renoux et al. 2000; Ni et al. 2022). Other compounds, such as CL-20, have also shown toxicity for Eisenia species (Robidoux et al. 2004d).
For earthworms exposed to naturally contaminated soils by PAHs, such as clay-target impacted soils, a lower PAH bioavailability was observed (Rodríguez-Seijo et al. 2017) since PAHs bioavailability is highly dependent on organic matter content and earthworms can increase contact of PAHs degrading soil microorganisms with the contaminant (Dendooven et al. 2011; Rodríguez-Seijo et al. 2017). However, Esmaeli et al. (2022) recently reported that PAH accumulation increased significantly in species with burrowing habits, and gut uptake is the main route of PAHs exposure. Other parameters, such as oxidative stress and worm reproduction, in general, seem to be impacted when exposed to contaminated soils by PAHs (Dendooven et al. 2011; Rodríguez-Seijo et al. 2017).
In general, some of these studies have usually been conducted with single contamination or the same kind of pollutants (only PTEs, explosive compounds, etc.), while studies with mixed contamination are scarce. This question requires special attention.
Other soil organisms from macrofauna
Gastropods, ants, ground beetles, and amphibians have also been studied, and effects on these communities are similar to those on earthworms. Kennedy et al. (2012) and Lindsay et al. (2017) assessed the impact of W on gastropods (Otala lactea). They observed that Na2WO4 is more toxic when exposed directly to organisms than when spiked with soils. In addition, these researchers observed that W could be accumulated in gastropods through cabbage (Brassica oleracea) ingestion, where W was bioaccumulated. The W is toxic, not inert to soil organisms, as shown for earthworms, and should be avoided.
Studies with ants also observed that military training highly impacts their abundance and diversity (species richness and equitability) in moderately or lightly disturbed areas (Graham et al. 2004, 2009), making them a valuable indicator for biomonitoring of military areas (Graham et al. 2008). Woinarski et al. (2002) reported that the abundance and richness of ants collected from military training areas and areas impacted by pastoralism were higher in areas subjected to military training than those impacted by grazing activities. Bryant (2010) also reported that ground beetle species richness and abundance did not differ between control and impacted areas by Pb and Sb derived from ammunition weathering.
Finally, Bazar et al. (2009) found that in amphibians, such as red-backed salamanders (Plethodon cinereus), survival rates were highly impacted by Cu levels over 1,333 mg kg−1 in the first days of exposure, while Johnson et al. (1999) observed that TNT can be bioaccumulated in tiger salamanders (Ambystoma tigrinum) through dermal exposure and via food (earthworms), as was indicated for gastropods (Kennedy et al. 2012; Lindsay et al. 2017).
Concluding remarks and prospects for future research
This review highlighted that more studies are needed with different biological levels, since exposure to the same contaminant can be different for soil microorganisms, micro-, meso- or macrofauna, and soil properties or uptake behaviour influence contaminant bioavailability. Data on combined exposures (e.g., PTEs and explosive-related compounds) are scarce, since most studies focused on single contamination, usually Pb, when combined contamination would be more realistic. A similar problem was detected for Pb-free ammunition, where more studies are required since Bi or W could have similar toxicity to Pb for soil organisms.
Studies conducted on clay target shooting ranges should also consider PAHs while firing ranges or military areas should assess a wide range of PTEs and organic contaminants, depending on the types of ammunition used and carried activities. This consideration is critical for laboratory studies as well, where assessing combined exposures could provide more realistic insights than single exposures. Additionally, laboratory studies should incorporate a broad range of concentration levels, especially at higher concentrations, since these areas can be highly polluted due to ammunition accumulation. Besides, other understudied impacts, such as mechanized military training activities or bombturbation, should also be assessed since changes in soil properties can influence organism abundance and soil biodiversity.
In warfare areas and military training areas, other potential contaminants, such as PFAs, should be considered (Skalny et al. 2021; Ruyle et al. 2023). Per- and poly-fluoroalkyl substances, commonly found influoropolymers, used in munitions for their ability to withstand high temperatures and pressures, can be released into the environment as aerosols after detonation (Koban and Pfluger 2023). Moreover, in the 1980s, single-use plastic casing and plastic wadding replaced waxed paper hulls for the vast majority of shotgun shells. Since then, plastic, usually extruded polyethene (both LDPE and HDPE) and polypropylene, has been the material universally adopted containing the projectiles or shots pellets (Rotter et al. 2022). However, plastics in the field can suffer a similar process to ammunition weathering, and some microplastics could be released into the environment, which could also represent an environmental issue for biota. Kanstrup and Balsby (2018) and Bimrose et al. (2020) found plastic litter from hunting ammunition associated with wetland hunting. However, this has not been studied in soils yet. To avoid these issues, some manufacturers introduced biodegradable shotgun cartridges or biodegradable clay targets composed of natural resin or bioplastics (i.e. polyhydroxyalkanoates, potato starch, etc.). However, full plastic biodegradation is rarely achieved in the field and can have similar issues to the environmental biota (Zimmermann et al. 2020; Liwarska-Bizukojc 2021; Nik Mut et al. 2024).
Finally, the ammunition contaminants can have short to medium-term impacts on soil organisms. Therefore, during the shooting activities, environmental measures such as sieving for final stop cleaning or remediation measures, as well as using nets to collect ammunition and clay target remnants during and after shooting activities, are crucial for reducing ammunition weathering and mitigating potential environmental impacts.
Data availability
The authors confirm that the data supporting the findings of this study are available within the article.
Abbreviations
- 2,4-DANT:
-
2,4-Diamino-6-nitrotoluene
- 2,4-DNT:
-
2,4-Dinitrotoluene
- 2,6-DANT:
-
2,6-Diamino-4-nitrotoluene
- 2-ADNT:
-
2-Amino-4,6-dinitrotoluene
- 4A-2,6-DNT:
-
4-Amino-2,6-dinitrotoluene
- 4-ADNT:
-
4-Amino-2,6-dinitrotoluene
- CAT:
-
Catalase
- CL-20:
-
Hexanitrohexaazaisowurtzitane (China Lake compound 20, CL-20)
- CWAs:
-
Chemical warfare agents
- DHA:
-
Dehydrogenase
- DNAN:
-
2,4-Dinitroanisole
- DNB:
-
Dinitrobenzene
- DU:
-
Depleted Uranium
- GST:
-
Glutathione S-transferase
- HDPE:
-
High-density polyethylene
- HMX:
-
1,3,5,7-Tetranitro-1,3,5,7-tetrazocane
- LDPE:
-
Low-density polyethyleneNFA: Nitrogen-fixation activity
- NG:
-
Nitroglycerine
- NQ:
-
Nitroguanidine
- NRRT:
-
Neutral red retention time
- NTO:
-
Nitrotriazolone
- PAHs:
-
Polycyclic aromatic hydrocarbons
- PCBs:
-
Polychlorinated biphenyls
- PFAs:
-
Per- and polyfluoroalkyl substances
- PLFAs:
-
Phospholipid-derived fatty acids
- PNA:
-
Potential nitrification activity
- PTEs:
-
Potentially Toxic Elements
- RDX:
-
Hexahydro-1,3,5-trinitro-1,3,5-triazine
- SOD:
-
Superoxide dismutase
- TAT:
-
Triaminotoluene
- TNB:
-
1,3,5-Trinitrobenzene
- TNT:
-
Trinitrotoluene
- TPH:
-
Total petroleum hydrocarbons
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Acknowledgements
The authors would like to recognize the financial support of the Consellería de Cultura, Educación e Universidade (Xunta de Galicia) through the contract ED431C2021/46-GRC granted to the research group BV1 of the University of Vigo. ARS is supported by a JdCi research contract (IJC2020-044197-I) funded by MICIU/AEI/https://doi.org/10.13039/501100011033 and European Union EU/PRTR. DAL also acknowledge Ministerio de Ciencia e Innovación of Spain and the University of Vigo for his Juan de la Cierva Incorporación 2019 contract (IJC2019-042235-I) and RyC contract (RYC2022-036752-I) funded by MICIU/AEI/https://doi.org/10.13039/501100011033 and European Union EU/ESF+ . Funding for open access charge: Universidade de Vigo/CISUG. Finally, we would like to thank reviewers for taking the time and effort necessary to review and improve this manuscript.
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Rodríguez-Seijo, A., Fernández-Calviño, D., Arias-Estévez, M. et al. Effects of military training, warfare and civilian ammunition debris on the soil organisms: an ecotoxicological review. Biol Fertil Soils (2024). https://doi.org/10.1007/s00374-024-01835-8
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DOI: https://doi.org/10.1007/s00374-024-01835-8