Negative impacts of mining on Neotropical freshwater fishes

Valter M. Azevedo-Santos1 , Marlene S. Arcifa2 , Marcelo F. G. Brito3 , Angelo A. Agostinho4 , Robert M. Hughe5,6 , Jean R.S. Vitule7 , Daniel Simberloff8 , Julian D. Olden9 and Fernando M. Pelicice10

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Abstract​


EN

Mining activities have significantly affected the Neotropical freshwater ichthyofauna, the most diverse in the world. However, no study has systematized knowledge on the subject. In this review, we assembled information on the main impacts of mining of crude oil, gold, iron, copper, and bauxite on aquatic ecosystems, emphasizing Neotropical freshwater fishes. The information obtained shows that mining activities generate several different disturbances, mainly via input of crude oil, metals and other pollutants, erosion and siltation, deforestation, and road construction. Mining has resulted in direct and indirect losses of fish diversity in several Neotropical waterbodies. The negative impacts on the ichthyofauna may change the structure of communities, compromise entire food chains, and erode ecosystem services provided by freshwater fishes. Particularly noteworthy is that mining activities (legal and illegal) are widespread in the Neotropics, and often located within or near protected areas. Actions to prevent and mitigate impacts, such as inspection, monitoring, management, and restoration plans, have been cursory or absent. In addition, there is strong political pressure to expand mining; if – or when – this happens, it will increase the potential of the activity to further diminish the diversity of Neotropical freshwater fishes.

Keywords: Deforestation, Mercury, Oil spill, Roads, Silting.

PT

As atividades de mineração têm impactado significativamente a ictiofauna de água doce Neotropical, a mais diversa do mundo. Porém, nenhum estudo sistematizou o conhecimento sobre o assunto. Nesta revisão, reunimos informações sobre os principais impactos da mineração de petróleo, ouro, ferro, cobre, e bauxita sobre os ecossistemas aquáticos, com ênfase nos peixes de água doce Neotropicais. As informações obtidas mostram que as atividades de mineração geram diferentes distúrbios, principalmente por meio de petróleo bruto, metais e outros poluentes, erosão e assoreamento, desmatamento e construção de estradas. A mineração resultou em perda direta e indireta de diversidade de peixes de vários corpos d’água Neotropicais. Os impactos negativos sobre a ictiofauna podem alterar a estrutura das comunidades, comprometer cadeias alimentares inteiras, bem como degradar os serviços ecossistêmicos fornecidos pelos peixes de água doce. Particularmente importante é que as atividades de mineração (legais e ilegais) são generalizadas na região Neotropical, e frequentemente estão localizadas dentro ou perto de áreas protegidas. Ações de prevenção e mitigação de impactos, como planos de fiscalização, monitoramento, manejo e restauração, têm sido precárias ou ausentes. Além disso, há forte pressão política para expandir a mineração; se – ou quando – isso acontecer, aumentará o potencial da atividade em diminuir ainda mais a diversidade de peixes de água doce Neotropicais.

Palavras-chave: Assoreamento, Derramamento de óleo, Desmatamento, Estradas, Mercúrio.

Introduction​

The Neotropical realm supports the greatest known diversity of freshwater fish in the world, including over 6,000 described species (Albert et al., 2020). These fishes vary considerably in length, from mere centimeters to meters (Ferraris Jr., 2003; Castro, Polaz, 2020), and they display complex biogeographic patterns at multiple spatial extents. Freshwater fishes from the Neotropical region also display disproportionally high functional diversity (Toussaint et al., 2016), perform critical ecological functions (Reys et al., 2009), and provide many important ecosystem services, particularly artisanal and commercial fisheries (e.g., Isaac et al., 2015). Fish are also used in countless products such as jewelry and other objects (Olden et al., 2020), contribute to medicinal treatments (Alves, Rosa, 2006), and provide many other services. This rich biodiversity, however, has been eroded, degraded, or threatened with extinction (Reis et al., 2016; Pelicice et al., 2017; Vitule et al., 2017; ICMBio, 2018).

Mining is one of several activities that have affected Neotropical fish diversity (Pelicice et al., 2017). Mining extracts various materials (e.g., sand, oil, metals) and is conducted near or within waterbodies, generating a variety of wide-ranging negative consequences. For instance, successive oil spills from petroleum wells or pipelines in the Amazon basin (especially in Peru) have damaged fish assemblages in several rivers (Azevedo-Santos et al., 2016; Fraser, 2016). Another emblematic example was the recent rupture of tailings dams in southeastern Brazil, when toxic mine waste flowed into the Doce River and dramatically affected fish diversity (Fernandes et al., 2016; Weber et al., 2020). These are just a few examples of how mine operations and failures negatively affect freshwater ecosystems, including large-scale fish kills and biodiversity losses. Despite recent catastrophes that expose the dangers of mining operations (e.g., Fernandes et al., 2016; Olden et al., 2019), many Neotropical nations have largely downplayed the negative and pervasive impacts of mining. This is certainly the case for Brazil, where mining is widespread and plans exist for expansion and changes in legislation favoring the mining sector (Meira et al., 2016; Congresso Nacional, 2020).

The science to inform mining policy in the Neotropical region is available in published journals, grey literature (often internal mining company reports), and the news media, yet it has not been synthesized to facilitate an understanding of mining impacts on the Neotropical ichthyofauna. To address this knowledge gap, we systematically reviewed current knowledge regarding the main negative impacts of mining on Neotropical freshwater fishes. Several types of mining have related consequences. For example, gold mining results in input of toxic metals (e.g., Malm, 1998), which also occurs with petroleum production (e.g., Baqué, Doyle, 2017). Thus, we list the main impacts of mining of crude oil, gold, iron, copper, and bauxite. We chose these ores because there is more available information of negative impacts related to them. Although the negative effects of mining can be pervasive across taxonomic groups (e.g., Callisto et al., 1998a; Brosse et al., 2011), in this review we explore the impacts that can arise from inputs of crude oil and heavy metals and other pollutants, sediment erosion and siltation, deforestation practices, and road construction on Neotropical freshwater fishes.


Main consequences and negative impacts on fishes

Mining is a necessary activity for human societies. We depend on petroleum for transporting people and commodities, for example, and metals are a key component of human civilizations. However, mining has also proven to cause countless negative environmental impacts (e.g., Callisto et al., 1998a,b; Brosse et al., 2011; Hughes et al., 2016; Marrugo-Negrete et al., 2018; Albuquerque et al., 2020) that can be avoided or minimized. In this section, we review how different mining activities lead to detrimental impacts on Neotropical freshwater fishes.

Input of crude oil. Oil extraction and transportation are major economic activities, and oil spills resulting from poor mining practices are not uncommon (e.g., Sebastián, Hurtig, 2004; Hughes et al., 2016). Crude oil spills in Neotropical waterbodies have occurred repeatedly during or after the extraction (in the blocks) or in the transport via pipelines, latter associated with human actions (e.g., vandalism – including terrorism, poor maintenance) or environmental sources (i.e., natural catastrophes). In the Peruvian Amazon alone, more than 400 leaks were recorded over 19 years (León, Zúñiga, 2020), and many hundreds more occurred but were not reported or even discovered. The scenario is more complicated if we consider other countries (e.g., Ecuador) that extract oil in the region. Most instances of oil spills are poorly documented in the scientific literature, and effects on fish assemblages are substantially underreported. In addition to accidental spill events, crude oil was also intentionally released into ecosystems, likely reaching freshwater ones (Kimerling, 2006).

The environmental implications of oil spills on Neotropical freshwater fishes remain poorly documented (e.g., Fraser, 2016). However, in the Amazon basin, oil spills are frequent, resulting in dramatic impacts to fish assemblages (Fig. 1). Several oil spills have caused fish mortality (see Tab. 1) and have led to the accumulation of crude oil in organisms and in the freshwater environments (e.g., Fig. 1). The Marañón River basin, an important region for fishing (Coomes et al., 2010), has been the recipient of successive crude oil spills that have killed many fishes (Tab. 1).

The negative impacts of oil spills directly or indirectly related to petroleum activities extend beyond the Amazon River basin. A highly damaging case occurred in Brazil, where a crude oil spill was dumped in a stream, later reached the Barigui River, and flowed to the Iguaçu River (South Brazil), resulting in massive mortality (Tab. 1; see also Ostrensky et al., 2003). The Iguaçu River is the main waterbody of the Iguaçu River basin, where more than 50% of fish species are endemic (Zawadzki et al., 1999). Thus, oil spills in these Neotropical ecosystems (e.g., Iguaçu, Amazon basins) have probably impacted several endemic fish species, including those not described yet. Even in cases where there is no clear evidence of impacts on fish diversity (e.g., in Tab. 1), they possibly occurred at some level. For example, Short (2003) argued that oil contains the life-damaging chemicals “polycyclic aromatic hydrocarbons (PAH)”, and that these compounds negatively affect salmonid embryogenesis. In general, exposure to crude oil can have different non-lethal effect, such as impairing swimming capacity, and can result in malformations (Carls et al., 1999). Studies also show that fish exposed to petroleum have become more susceptible to parasitism (Khan, 1990) and eye and cardiac dysfunctions (Cherr et al., 2017; Magnuson et al., 2020). Thus, oil spills will not always have immediately visible effects on fishes, but they can affect individuals and populations for a long time.

TABLE 1 | Reports on crude oil spills in Neotropical waterbodies – also including those with negative impacts on fish diversity (based on Methods and Search results in S1A and S1B, respectively).

WaterbodiesCountryYear of spillAmount (liters)Negative impacts on fish diversity
Andean River to Lake TiticacaBolivia2000~4,734,642Yes
Stream to the Barigui and after to the Iguaçu RiverBrazil2000~4,000,000Yes
Catatumbo River to Lake MaracaiboColombia (effects in Venezuela)2001~2,861,771Possibly
Coatzacoalcos RiverMexico2004~794,937Possibly
Coatzacoalcos RiverMexico2011~238,481Yes
Catatumbo River to Lake MaracaiboColombia (effects in Venezuela)2012UnknownYes
Guarapiche RiverVenezuela2012~10,175,204 to ~19,078,508Yes
Coca RiverEcuador (effects in Peru)2013~1,825,174Possibly
Lake – Unknown namePeru2014UnknownYes
A tributary of the Marañón River basinPeru2014~254,380Yes
Stream – Unknown namePeru2014UnknownYes
Stream – Unknown nameBrazil2015~600Possibly
Chiriaco and Morona Rivers – 1Peru2016~476,962Possibly
Chiriaco and Morona Rivers – 2Peru2016UnknownPossibly
Stream – Unknown namePeru2016UnknownPossibly
Tepeyac stream and Coatzacoalcos RiverMexico2018UnknownYes
Streams, Sogamoso and Magdalena RiversColombia2018~79,494 to ~87,443Yes
Coca and Napo RiversEcuador (effects in Peru)2020~2,384,809Yes
Godineau RiverTrinidad and Tobago2020UnknownPossibly
Shiripuno RiverEcuador2020UnknownPossibly

Negative impacts on fishes may substantially perturb food webs (Azevedo-Santos et al., 2016) and diminish environmental services (e.g., fish as food). For example, traditional human communities have reported that water bodies affected by crude oil experienced a notable decline in fish diversity (Sebastián, Hurtig, 2004), with subsequent but unstudied impacts on fishery production. As fishes disperse seeds (Correa et al., 2007; Reys et al., 2009), this is, for instance, another affected service. In fact, all consequences (e.g., input of metals,chlorides, cyanides, roads) of different mining activities reported here will affect food webs and ecosystem services.

Another common problem, especially in the Amazon basin, is oil extraction in headwater areas (Finer et al., 2008), implying that local spills can often extend downstream to other sites (Azevedo-Santos et al., 2016, 2019), pervasively affecting fish diversity and fisheries activities. This effect was recently observed in the Magdalena River in Colombia and in other Neotropical regions (Tab. 1).

FIGURE 1 | Dead fishes (characiforms, cichliforms, and siluriforms) after crude oil spilled in waterbody of the Amazon River basin. Credits to Barbara Fraser.

After the input of massive amounts of a substance, especially in flowing waters, recovering the substance is difficult. In this case, petroleum, in addition to reaching downstream areas, remains present in aquatic organisms and sediment (e.g., Fig. 1); this persistence was verified after the oil spill resulting from the Deepwater Horizon accident (Liu, Liu, 2013). Therefore, freshwater fish from Amazonia and other Neotropical regions where leaks have occurred can be exposed to the negative effects of crude oil for months or years.

Input of metals. Different metals associated with mining operations can leach directly into watersheds; the volume and rate of the leaching are often unknown. Activities involved in the extraction of crude oil, gold, iron, and copper cause input of minerals into waterbodies. Some minerals have contaminated or otherwise affected Neotropical freshwater fishes (Tab. 2) – including in Amazonian systems, where small-scale mining activities, many of them illegal, are widespread. The sources of minerals in freshwater ecosystems are well known and include the failure of tailings disposal facilities and the chronic release of minerals during mining operations.

Many mines have tailings disposal facilities (hereafter TDFs; see fig. 1 in Salvador et al., 2020) that are used when large volumes of metal ores are mined (Tab. 3). The tailings may include finely ground rock (silt, powder), metals (e.g., cadmium), and processing chemicals and slimes, some of which are toxic (e.g., cyanides). These facilities are vulnerable to various disruptions (Nazareno, Vitule, 2016). When they collapse, TDFs release huge masses of toxic tailings, silt, and very turbid water into downstream environments (e.g., streams, rivers, floodplains, estuaries), causing extensive environmental changes. Numerous collapses of TDFs are reported in Neotropical countries (e.g., Wise, 2020), some of which have been highly publicized in popular media – especially when people died. However, for many of these cases little is known about the true magnitude of the impact of the accident on fishes, especially for events occurring before the 1990s.

In Brazil, TDF failures have resulted in catastrophic biodiversity losses in important rivers. The best-known examples, because of their social impacts and biodiversity losses, were the ruptures of the Fundão and Brumadinho TDFs, both in the State of Minas Gerais (Lambertz, Dergam, 2015; Fernandes et al., 2016; Cionek et al., 2019). In the case of Fundão, the refuse flowed downstream in the Doce River, in the southeastern part of Brazil (Carmo et al., 2017). This single event may have killed endemic, threatened, and undescribed fish species (Fernandes et al., 2016). The Brumadinho TDF rupture affected another major waterbody, the Paraopeba River, in the São Francisco River basin (Cionek et al., 2019), killing a huge number of fish. These events immediately changed limnological conditions and imported high levels of toxic mud (i.e., metals were present; Fernandes et al., 2016), impacting fishes. For example, the fish Danio rerio (Hamilton, 1822), exposed to the water from an affected waterbody (i.e., Paraopeba River), manifested high percentages of dead embryos or specimens with abnormalities (Thompson et al., 2020). In both cases, metals but also mud and other compounds in the TDF may have played a central role in the massive fish kill (Fernandes et al., 2016; Vergilio et al., 2020). Despite these catastrophes, Brazil currently has > 500 TDFs (Nazareno, Vitule, 2016), which may substantially damage ecosystems and fish diversity if – or when – they fail.

Metal inputs into Neotropical freshwaters also occur via other routes, including the deliberate or accidental release of effluents into waterbodies. Many rivers of different nations (e.g., Bolivia, Ecuador, French Guiana, Peru) probably received mercury during gold mining (Tab. 2), including many watercourses in the Amazon basin. Most contamination is likely related to illegal mining, a frequent activity in many Neotropical nations. These actions have led to extensive contamination, with likely lethal and sub-lethal effects on organisms. For instance, considerable research points to mercury in fish and in the environment of many Amazon rivers (Tab. 2). Mercury can cause genetic modification (Porto et al., 2005), brain disorders (Peterson et al., 2007), and other toxic effects (Monteiro et al., 2017). Furthermore, because it is a toxic metal with bioaccumulation potential (Morel et al., 1998), mercury usually accumulates and, through the trophic transfer, may harm entire food webs, from smaller fish to top predators (e.g., Salminus spp., Hoplias spp., Cichla spp., Caiman crocodilus), including large mammals (e.g., Trichechus inunguis) and humans (Malm, 1998).

TABLE 2 | Neotropical freshwater fishes affected by metals in regions with records of mining activities (Methods in S2).

MiningPollutantWaterbodyCountryReferences
CopperVarious metalsJoão Dias StreamBrazilAbril et al. (2018a,b)
GoldMercuryTributaries of the Amazon basinBrazilAkagi et al. (1995)
GoldMercuryMagdalena RiverColombiaAlvarez et al. (2012)
GoldMercuryPiracicaba RiverBrazilArantes et al. (2009)
GoldMercuryParaíba do Sul RiverBrazilAzevedo et al. (2017)
GoldMercuryMadeira RiverBrazilBastos et al. (2006, 2015); Bataglioli et al. (2019)
GoldMercuryTartarugalzinho River basinBrazilBidone et al. (1997a)
GoldMercuryTapajós RiverBrazilBidone et al. (1997b)
GoldMercurySinnamary River basinFrench GuianaBoudou et al. (2005)
GoldMercuryTapajós River basinBrazilBrabo et al. (2000)
GoldMercuryMadeira RiverBrazilDórea et al. (1998); Braga et al. (2015)
GoldMercuryTapajós River basinBrazilCastilhos et al. (1998); Faial et al. (2015)
GoldMercuryPetit-Saut reservoir (Sinnamary River basin)French GuianaDurrieu et al. (2005)
GoldMercuryMadre de Dios River basinPeruFeingold et al. (2020)
GoldMercuryParaguay RiverBrazilFerreira et al. (2017)
GoldMercuryUpper Maroni RiverFrench GuianaFréry et al. (2001)
GoldMercuryLake TiticacaPeruGammons et al. (2006)
GoldMercurySeveral waterbodiesFrench GuianaGentès et al. (2019)
GoldMercuryTeles Pires River and Cristalino RiverBrazilHacon et al. (2000)
GoldMercuryParaguay River basinBrazilHylander et al. (2000)
GoldMercuryRivers of Amazon basinBrazilKehrig, Malm (1999)
GoldMercuryParaguay River basinBrazilLeady, Gottgens (2001)
GoldMercuryPiriá River and Grande LakeBrazilLima et al. (2005)
GoldVarious metalsCassiporé River basinBrazilLima et al. (2015)
GoldMercuryTapajós River basinBrazilMalm et al. (1995); Lino et al. (2019)
GoldMercurySeveral tributaries of Amazon basinBrazilMalm (1998)
GoldMercuryCauca and San Jorge River basinsColombiaMarrugo-Negrete et al. (2018)
GoldMercuryMalinowski RiverPeruMartinez et al. (2018)
GoldMercuryFrench Guiana riversFrench GuianaMaury-Brachet et al. (2020)
GoldMercuryLake ManaguaNicaraguaMcCrary et al. (2006)
GoldMercuryCoastal riversSurinameMol et al. (2001)
GoldMercuryRivers of Cuyuní River basinVenezuelaNico, Taphorn (1994)
GoldMercuryMagdalena RiverColombiaOlivero, Solano (1998)
GoldMercuryAtrato RiverColombiaPalacios-Torres et al. (2018)
GoldVarious metalsAtrato RiverColombiaPalacios-Torres et al. (2020)
GoldMercuryCoastal riversBrazilPalheta, Taylor (1995)
GoldMercuryMadeira and Paraíba do Sul River basinsBrazilPfeiffer et al. (1989); Pfeiffer et al. (1991)
GoldMercuryTucuruí Reservoir and Moju RiverBrazilPorvari (1995)
GoldMercuryIténez RiverBoliviaPouilly et al. (2012, 2013)
GoldMercuryMutum-Paraná and Madeira RiversBrazilReuther (1994)
GoldMercuryTapajós RiverBrazilSantos et al. (2000, 2002)
GoldMercurySolimões River basinBrazilSilva, Lima (2020)
GoldMercurySolimões RiverBrazilSilva et al. (2019)
GoldMercuryMadeira RiverBrazilSoares et al. (2018)
GoldMercuryBacajá RiverBrazilSouza-Araujo et al. (2016)
GoldMercuryPuyango River basinEcuadorTarras-Wahlberg et al. (2001)
GoldMercuryTapajós River basinBrazilUryu et al. (2001)
IronVarious metalsDoce RiverBrazilFernandes et al. (2016); Ferreira et al. (2020); Macêdo et al. (2020); Weber et al. (2020)
IronVarious metalsParaopeba RiverBrazilThompson et al. (2020); Vergilio et al. (2020)

Another source of metal pollution, especially in the Amazon basin, is through oil extraction. In general, petroleum extraction involves the presence of water contaminated by heavy metals (Baqué, Doyle, 2017). Known as “produced water”, this refuse has been released directly into waterbodies (Ibáñez, 1997; see also next subsection), as has been recorded in rivers from Colombia (Avellaneda, 1990), Ecuador (Ibáñez, 1997), and Peru (Baqué, Doyle, 2017). It is likely that the same input occurs in other Neotropical countries with high oil extraction activity (e.g., Venezuela). According to León, Zúñiga (2020:39), in only two areas of oil production in the Amazon, “approximately 408 million barrels” were generated in a single year and likely reached nearby waterbodies. The impacts of this waste on fish are unclear, as they have not been adequately examined. It is known that in regions where this waste was released, fish assemblages were contaminated by “copper, lead, zinc and mercury” (Baqué, Doyle, 2017:61). Other reports indicate that aquatic life was devastated in the presence of this waste (Ibáñez, 1997). It is likely that part of these effects is related to the presence of metals in the water, but other substances (e.g, chloride) may also be involved.

As with spills of crude oil and other substances, the release of metals, especially in high quantities, permeates entire river systems and affects fishes in adjacent environments and downstream habitats. This process was well documented in the failure of the Mariana TDF, which first contaminated a small watercourse, then spread through the mainstem of the Doce River (Fernandes et al., 2016; Carmo et al., 2017) and reached estuarine and marine ecosystems (Andrades et al., 2020). In fact, the problem of propagation of disturbances from headwater to downstream pervades all consequences of mining activities, including input of chemicals, deforestation, erosion and siltation, and roads, because these disturbances may occur in the upper sections of the watershed.

TABLE 3 | Major tailings disposal facilities (TDFs) that collapsed – with reports of effects on Neotropical freshwater fishes (Methods in S3).

MiningDecade of collapseRiver affected (country)References
Lead and zinc1990Pilcomayo River (Bolivia)Garcia-Guinea, Harffy (1998)
Gold1990Omai River (Guyana)Vick (1996)
Bauxite2000Murucupi River (Brazil)Silva et al. (2012)
Iron2010Doce River (Brazil)Fernandes et al. (2016)
Iron2010Paraopeba River (Brazil)Cionek et al. (2019); Thompson et al. (2020);
Vergilio et al. (2020)

Input of cyanides. Gold mining activities in different Neotropical countries, for example, Argentina, Costa Rica, French Guiana, Guatemala, Mexico, Nicaragua, Panama, and Suriname, have been reported to use cyanide. In the Neotropical region, cyanide is used in both legal and/or illegal mining activities. For instance, in Minas Gerais (Brazil), the Mina do Engenho had dams with cyanide (S4). An example of the illegal use is the case of Costa Rica, in Central America. In this country, in 2019, an enforcement operation seized more than two tons of the product in an illegal mining area (S5).

When this pollutant reaches a water body – owing to the rupture of dams, rain, deliberate disposal, or other reasons – freshwater fishes are affected (Tab. 4). The main problem is that effluents containing the substance often end up in waterbodies (Caheté, 1998) – despite few scientific reports documenting occurrences. For example, a tributary of the Jáchal River basin in Argentina was contaminated by cyanide after a spill, but the effects on fish are still unclear. Other examples occurred in Mexico, where high cyanide concentrations reached the Piaxtla River and killed several immature fish (Tab. 4), and Honduras, where successive accidents introduced cyanide into the Lara River; in the latter case, there was a strong negative impact on the ichthyofauna (Tab. 4). These kills may occur for different reasons, including difficulty in breathing owing to the presence of the substance (Eisler, 1991).

Cyanides may affect fishes in different ways. As argued by Eisler (1991:27), “(…) adverse effects of cyanide on fish include delayed mortality, pathology, impaired swimming ability and relative performance, susceptibility to predation, disrupted respiration, osmoregulatory disturbances, and altered growth patterns”. These problems may also have afflicted assemblages of the recorded disasters (Tab. 4). Immature forms may suffer the effects of these substances. For example, Leduc (1978) exposed Salmo salar Linnaeus, 1758, to hydrogen cyanide (HCN), a compound that may be also present in the mining. This author observed external changes in egg color and delayed hatching. For larvae, Leduc (1978) observed that the exposure to hydrogen cyanide resulted in morphological changes. This suggests that, in environments affected by cyanide, the recruitment of fish populations was also severely affected. In addition, the impact may propagate along the food chain, because cyanides also affect plants and macroinvertebrates (Eisler, 1991). Thus, the trophic structure of the entire community may be affected.

Input of chlorides, salts, polycyclic aromatic hydrocarbons (PAH). Produced waters extracted during oil extraction – in addition to metals (see subsection “Input of metals”) – also contain other substances (Neff et al., 2011;Baqué, Doyle, 2017; Yusta-García et al., 2017). As mentioned, produced waters were dumped into many tributaries in the Amazon basin; for instance, the Corrientes, Pucacungayacu, Manchari, and Tigre Rivers (Yusta-García et al., 2017; see figures in Baqué, Doyle, 2017:59 and 61). There are reports of losses of Neotropical fish diversity from produced water (Ibáñez, 1997). Chloride, high levels of salts, and polycyclic aromatic hydrocarbons (PAH)(Neff et al., 2011) may play a role in the negative impacts on freshwater organisms. One impact may be due to the “chlorinity” effect in areas where produced waters are dumped (Kimerling, 2006:453). Ibáñez (1997) and Kimerling (2006) argued that this phenomenon may chemically block ecosystems and affect the routes used by the ichthyofauna during migration and spawning events. However, we emphasize that these effects (barriers) should be better evaluated.

The saline compounds, according to Neff et al. (2011), probably include sodium chloride (NaCl). Hintz, Relyea (2017) exposed rainbow trout Oncorhynchus mykiss (Walbaum, 1792) to this substance. Among their results, the authors showed that, depending on the concentrations of sodium chloride, individual growth was negatively affected. Similarly, PAHis expected to be highly damaging to freshwater fishes in both the short and long terms (see subsection “Input of crude oil”).

Erosion and siltation. Mining activities (iron, bauxite, gold, and copper) cause erosion and/or siltation in nearby waterbodies (e.g., Lin, Caramaschi, 2005; Nascimento et al., 2012; Verbete, 2012; Wantzen, Mol, 2013; Lobo et al., 2016; Melo et al., 2018), and in some cases the sediment may be contaminated by metals and other pollutants (Lopes et al., 2019). The extraction of other ores, like crude oil, may play a role in erosion and siltation (especially through deforestation and roads). These processes can have direct or indirect negative effects on fish. Erosion and siltation affect fish physiology, such as gill functioning (Wantzen, Mol, 2013). Other impacts include reduced water quality, loss of environmental heterogeneity, and altered habitats for fish feeding, refuge, reproduction, and development (Mol, Ouboter, 2004; Wantzen, Mol, 2013), especially through impacts on substrate interstices, leaf pack sedimentation, and aquatic plants. In a study evaluating the effects of erosion from a gold mine in Suriname, Mol, Ouboter (2004) showed that mining increased water turbidity with eroded material released from the mine. In addition, they reported “low habitat diversity, and a fish community with reduced diversity, few young fishes, and many fishes adapted to low light” (Mol, Ouboter, 2004:210). Erosion also contributes to the entry of mercury present in soil into the aquatic ecosystem, causing fish contamination (Richard et al., 2000). Another important case of siltation occurred in a lake in the Brazilian Amazon. Bauxite mining effluents, which include clay, were deposited for a decade in Lake Batata, in the Trombetas River basin (Bozelli, 1994; Lin, Caramaschi, 2005), and likely caused effects on fish diversity (Lin, Caramaschi, 2005).

In general, additional research is needed to better elucidate the negative impacts of siltation resulting from different mining activities on Neotropical fishes. However, silting from other human activities (Tab. 5) may serve as a baseline to predict the impacts of silting from mining. Inputs of sediments into aquatic environments resulting from anthropogenic actions have been incorporated into species extinction risk assessments (ICMBio, 2018). For example, silting is among the negative impacts listed to justify the classification of Brycon vermelha Lima & Castro, 2000, an endemic Brazilian fish, as endangered on the Brazilian red list (Santos et al., 2018). We emphasize that sediments from mining may carry metals (Lopes et al., 2019), which further increases the likelihood of adverse effects on freshwater fishes.

Deforestation. Mining activities (crude oil, gold, iron, copper, and bauxite) are also responsible for expanding deforestation (Kimerling, 2006; Swenson et al., 2011; Sonter et al., 2017; Espejo et al., 2018; Melo et al., 2018; Dethier et al., 2019; Diringer et al., 2020), directly or indirectly. For example, after a global crisis in the 2000s that affected several economies, the value of gold increased and, consequently, deforestation increased also in several Neotropical countries (Alvarez-Berríos, Aide, 2015) – indicating a strong correlation between mining and removal of vegetation.

TABLE 4 | Reports of cyanide spills due to mining in Neotropical region – including those with negative impacts on fish diversity (based on Methods and Search results in S6A and S6B, respectively).

WaterbodiesCountryYear of spillAmount (liters)Negative impacts on fish diversity
Bambana RiverNicaragua1978UnknownPossibly
Omai and Essequibo RiversGuyana1995~1,230,258,830 to ~3,000,000,000Yes
Several waterbodiesPanama1998UnknownPossibly
Lara RiverHonduras2003UnknownYes
Lara RiverHonduras2009~568Yes
San Sebastián RiverEl SalvadorUnknownUnknownPossibly
Puyango-Tumbes RiverEcuadorUnknownUnknownPossibly
Tributary of Velhas RiverBrazil2011UnknownYes
Several waterbodiesArgentina20151,000,000Possibly
Piaxtla RiverMexico2018200Yes
Tapajós RiverBrazil2018UnknownPossibly

TABLE 5 | Examples of negative effects of siltation on Neotropical freshwater fishes (Methods in S7).

Siltation reasonDisturbanceCountryReferences
PastureDecrease of the integrity of fish assemblagesBrazilCasatti (2004)
AgricultureAffect negatively the functional diversityBrazilDala-Corte et al. (2016)
MiningDecrease in fish diversityBrazilLin, Caramaschi (2005)
MiningReduction of fish diversitySurinameMol, Ouboter (2004)

The negative impact of deforestation from other activities (e.g., conversion to pasture) on fish diversity is known (Tab. 6). However, negative effects of deforestation arising from mining require more research in Neotropical regions. In general, deforestation of riparian vegetation has resulted in strong changes in the ichthyofauna (e.g., Tab. 6). The negative effects include, for instance, changes in taxonomic and functional features (Casatti et al., 2012) and losses of species, especially those sensitive to impacts (Dala-Corte et al., 2016). These same effects – or perhaps worse, because of contamination by metals – may occur on fishes in areas deforested owing to mining activities.

Roads. Virtually all types of mining (including crude oil, gold, iron, copper, and bauxite) need roads to transport the extracted ores or inputs (e.g., cyanide).Therefore, the maintenance, rehabilitation, and construction of new roads are common processes in mining areas (Kimerling, 2006; Edwards et al., 2014). Construction of new roads is especially common in remote regions. For example, Texaco, the oil company, constructed long roads (> 600 km) in the Amazonian forest (Kimerling, 2006). New roads precipitate a sequence of disturbances from deforestation (e.g., Barber et al., 2014) to erosion process and silting (Kimerling, 2006), besides introducing barriers to fish dispersal in small waterbodies (Leitão et al., 2018). The reasons for road construction are varied (Edwards et al., 2014), but their impacts are similar. The most important aspect is that roads fuel mining and other activities, including illegal ones.

New roads cause direct deforestation and open opportunities for ancillary activities, such as logging, construction of settlements, and other types of occupation (Barber et al., 2014). In addition, they cause direct and indirect erosion (Smith et al., 2018). New roads also fragment aquatic habitats, and many studies (e.g., Belford, Gould, 1989; Mariano et al., 2012; Brejão et al., 2020) have demonstrated that road culverts hinder hinder the movement of fishes. For example, Makrakis et al. (2012) evaluated the negative impacts of culverts, showing that 90% of them seriously threat fish movements. Brejão et al. (2020), studying Amazonian streams, found that roads crossing these small waterbodies affected the distribution of ichthyofauna by fragmenting habitats. A case of roads constructed for mining that generated negative impacts on fishes was reported for the Amazon. Kimerling (2001:330) described how the company Occidental Petroleum constructed a road in the El Eden region, in Ecuador, that “blocked the migration of fish from a lake into seasonally flooded forest”.

Roads also directly or indirectly pollute aquatic ecosystems. For example, exploration for crude oil in Ecuadorian Amazonia resulted in roads coated with oil that, in turn, polluted several waterbodies with high fish diversity (Kimerling, 2006). Run-off may have generated several negative effects, lethal and non-lethal, on fishes (see subsection “Input of crude oil”). Another type of pollution may come from the usage of these roads for mining. An event that received prominence was the contamination of the Yaqui River, in Mexico (near the Neotropical limits), with cyanide (S9). The pollution occurred after an accident with a truck transporting the substance to a mine (S9). Cases like these are likely to occur frequently in the Neotropical region, but they are not reported to authorities and do not receive the attention of the media. Other types of pollution arising from roads are eutrophication processes (Smith et al., 2018), plastics (Windsor et al., 2019), and solid and liquid waste from traffic. These disturbances harm the aquatic biota.


A growing threat

Currently, political forces work to expand mining activities across Neotropical countries. In Brazil, particularly, plans are afoot to expand the activity across the country, especially in the Amazon, Southeast, and Northeast regions (Ferreira et al., 2014; Villén-Perez et al., 2017). The strong lobby of the mining sector has spurred revisions in Mining Code legislation (Meira-Neto, Neri, 2017). A direct result of this movement has been the creation of the National Mining Agency in 2017, which has increased the sector’s autonomy and political power against environmental restrictions. Moreover, the Brazilian Congress is currently analyzing bills that propose mining in protected areas and indigenous lands, in addition to a constitutional amendment that proposes simplifying the environmental licensing system (El Bizri et al., 2016; Villén-Perez et al., 2017; Congresso Nacional, 2020). Such simplification, if approved, will enable the construction/operation of large-scale projects, including mining, without the need for rigorous environmental assessments (Fearnside, 2016). The mining lobby strengthened after the election of President Jair Bolsonaro, who has defended a “development” agenda with little regard for the environment and sustainability (Azevedo-Santos et al., 2021; Thomaz et al., 2020; Pelicice, Castello, 2021) and with political and legal incentives for the agrarian and mining sectors (Campo-Silva, Peres, 2019). The president himself has expressed his desire to allow the exploration for mineral resources in protected areas and indigenous lands of the Amazon. Rather than these current activities, Brazil should play an important role in avoiding policies that erode the Neotropical ichthyofauna. This is because, based on recent publications on described species (ICMBio, 2018; Albert et al., 2020), we estimate that the country holds a little more than 50% of species richness of freshwater fishes of the Neotropics. Using other sources of information (ICMBio, 2018; Fricke, Eschmeyer, 2021), we suggest that Brazil harbors between 16 to 18% of the species richness of freshwater fishes of the planet. This is an extraordinarily high diversity for a single jurisdiction. This outsize role suggests that political action, for example, at the federal level to expand mining at any cost, can affect a considerable portion of the Neotropical freshwater fishes.

TABLE 6 | Examples of negative impacts of deforestation on Neotropical freshwater fishes (Methods in S8).

Deforestation typeDisturbanceCountryReferences
Agriculture and pasture Changes in densityEcuadorBojsen, Barriga (2002)
Pasture“Negative threshold responses”BrazilBrejão et al. (2018)
Pasture and agricultureAlterations in both taxonomic and functional featuresBrazilCasatti et al. (2012)
PastureChanges in species compositionBrazilCosta et al. (2020)
Pasture and agricultureAlterations in the size of fishesBrazilIlha et al. (2018)
AgricultureIncrease of abundance of some speciesBrazilIlha et al. (2019)
AgricultureChange in functional compositionBrazilLeitão et al. (2018)
Pasture and grassland“Functional changes”BrazilLobón-Cerviá et al. (2016)
PastureChanges in abundanceCosta RicaLorion, Kennedy (2009)
PastureChange in functional groupsBrazilTeresa et al. (2015)
PastureChanges in richness and abundanceBrazilVirgilio et al. (2018)

The trend of expanded mining activity has been observed in many other countries of the Neotropical region (Hammond et al., 2013) and will complicate the current scenario. Small-scale mining is widespread in Neotropical nations (Harlow et al., 2019), and many mines are located within protected areas (Kamino et al., 2020). In addition, illegal activities are frequent in remote regions, for example, in parts of Amazonia. Currently, inspection and monitoring of mining activities have been insufficient, while fines and sanctions for environmental damage have rarely been paid (especially in large-scale catastrophes), and emergency, management, and environmental restoration plans have been negligent, precarious, or absent (Cionek et al., 2019; Salvador et al., 2020). Further weakening legislation will reduce environmental restrictions and fuel the expansion of the activity, including in protected areas, where more than 10,000 projects await authorization (Villén-Perez et al., 2017). One important concern is the political influence of the mining sector, because mining companies have traditionally financed political campaigns, which has fueled corruption (Meira-Neto, Neri, 2017).

As mining activities – together with hydroelectric power plans (Winemiller et al., 2016) and other human actions (Pelicice et al., 2017, 2021; Tófoli et al., 2017; Daga et al., 2020; Mezzaroba et al., 2021) – expand in different nations, impacts on Neotropical biodiversity will become increasingly prominent. The maintenance of freshwater fish diversity in the region will depend on policies that regulate mining activities so that their expansion is balanced with the protection of ecosystems and biodiversity.


CONCLUSION

The diversity of Neotropical fishes, together with their ecosystem services, have been affected in different ways by mining activities. The main negative impacts come from input of crude oil, contamination by metals and other pollutants, erosion, silting, deforestation, and road construction. Some consequences, especially crude oil spills and the rupture of tailing dams, have brutal and long-lasting negative impacts on aquatic ecosystems. Although impacts are undisputable, there is a clear need for more scientific research. The present review demonstrated that the number of studies is still relatively small, and some impacts remain largely uninvestigated. The unpredictable nature of accidents, in particular, makes it difficult to plan studies, indicating the need for continuous and long-term monitoring of the fish fauna, especially in large or risky mining operations. Experimental and field studies are needed to fill important gaps concerning the response of fish to different consequences of mining activities.

The fact that mining activities damage the fish fauna should guide Neotropical countries to review their mining plans to establish more rigorous regulations and to adopt measures to contain illegal developments. We emphasize that some activities cause acute impacts in particular conditions (i.e., TDS spills), whereas others affect the environment continuously (e.g., gold mining), making it difficult to mitigate their effects. This fact increases the need for advances in inspection and monitoring programs, especially in areas where impacts have been reported and where they are likely to occur.


Acknowledgments​


We thank Barbara Fraser, for providing the Fig. 1. We are grateful to two anonymous reviewers and the editor for the suggestions that significantly improved this article. Fernando M. Pelicice, Marcelo F. G. Brito and Angelo A. Agostinho received research grants from CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico). Robert M. Hughes received a Fulbright Brasil grant.

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Authors


Valter M. Azevedo-Santos1 , Marlene S. Arcifa2 , Marcelo F. G. Brito3 , Angelo A. Agostinho4 , Robert M. Hughes5 , 6 , Jean R.S. Vitule7 , Daniel Simberloff8 , Julian D. Olden3  and Fernando M. Pelicice10 

[1]    Universidade Estadual Paulista, Instituto de Biociências, 18618-687 Botucatu, SP, Brazil. valter.ecologia@gmail.com (corresponding author).

[2]    Universidade de São Paulo, 14040-901 Ribeirão Preto, SP, Brazil. marcifa@usp.br.

[3]    Universidade Federal de Sergipe, Laboratório de Ictiologia, Departamento de Biologia, 49100-000 São Cristóvão, SE, Brazil. marcelictio@gmail.com.

[4]    Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais (PEA), Universidade Estadual de Maringá, PR, Brazil. agostinhoaa@gmail.com.

[5]    Amnis Opes Institute, Corvallis, OR, USA. hughes.bob@amnisopes.com.

[6]    Oregon State University, Department of Fisheries, Wildlife, & Conservation Sciences, Corvallis, OR, USA.

[7]    Universidade Federal do Paraná, Laboratório de Ecologia e Conservação, Departamento de Engenharia Ambiental, Setor de Tecnologia, Curitiba, PR, Brazil. biovitule@gmail.com.

[8]    Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, 37996, USA. dsimberloff@utk.edu.

[9]    Departamento de Oceanografia Biológica, Instituto OceanSchool of Aquatic and Fishery Sciences, University of Washington, Seattle, WA 98195, USA. olden@uw.edu.

[10]   Universidade Federal do Tocantins, Núcleo de Estudos Ambientais, 77500-000 Porto Nacional, TO, Brazil. fmpelicice@gmail.com.

Authors Contribution


Valter M. Azevedo-Santos: Conceptualization, Formal analysis, Methodology, Supervision, Writing-original draft, Writing-review and editing.

Marlene S. Arcifa: Methodology, Writing-original draft, Writing-review and editing.

Marcelo F. G. Brito: Methodology, Writing-review and editing.

Angelo A. Agostinho: Writing-review and editing.

Robert M. Hughes: Writing-review and editing.

Jean R.S. Vitule: Writing-review and editing.

Daniel Simberloff: Writing-review and editing.

Julian D. Olden: Writing-review and editing.

Fernando M. Pelicice: Writing-review and editing.

Ethical Statement​


Not applicable.

Competing Interests


The authors declare no competing interests.

How to cite this article


Azevedo-Santos VM, Arcifa MS, Brito MFG, Agostinho AA, Hughes RM, Vitule JRS, Simberloff D, Olden JD, Pelicice FM. Negative impacts of mining on Neotropical freshwater fishes. Neotrop Ichthyol. 2021; 19(3):e210001. https://doi.org/10.1590/1982-0224-2021-0001

Copyright​


This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Distributed under

Creative Commons CC-BY 4.0

© 2021 The Authors.

Diversity and Distributions Published by SBI

Accepted May 17, 2021 by Paulo Pompeu

Submitted January 1, 2021

Epub Sept 17, 2021