Gall, et al. 2015. Published in Environmental Monitoring and Assessment. 187:201 Transfer of heavy metals through terrestrial food webs: areview Jillian E. Gall & Robert S. Boyd & Nishanta Rajakaruna Abstract Heavy metals are released into the environ- metal-tolerant insects, which occur in naturally high- ment by both anthropogenic and natural sources. Highly metal habitats (such as serpentine soils) and have adap- reactive and often toxic at low concentrations, they may tations that allow them to tolerate exposure to relatively enter soils and groundwater, bioaccumulate in food high concentrations of some heavy metals. Some webs, and adversely affect biota. Heavy metals also metallophyte plants are hyperaccumulators of certain may remain in the environment for years, posing long- heavy metals and new technologies using them to clean term risks to life well after point sources of heavy metal metal-contaminated soil (phytoextraction) may offer pollution have been removed. In this review, we compile economically attractive solutions to some metal pollu- studies of the community-level effects of heavy metal tion challenges. These new technologies provide incen- pollution, including heavy metal transfer from soils to tive to catalog and protect the unique biodiversity of plants, microbes, invertebrates, and to both small and habitats that have naturally high levels of heavy metals. large mammals (including humans). Many factors con- tribute to heavy metal accumulation in animals includ- Keywords Ecosystem health . Metal toxicity. Metal ing behavior, physiology, and diet. Biotic effects of hyperaccumulation . Bioaccumulation . Environmental heavy metals are often quite different for essential and pollution . Phytoremediation non-essential heavy metals, and vary depending on the specific metal involved. They also differ for adapted organisms, including metallophyte plants and heavy Introduction Jillian E. Gall holds a BA, College of the Atlantic. Polluting vast areas worldwide, heavy metals are highly Robert S. Boyd holds a PhD, Auburn University. reactive and toxic at low concentrations, posing severe Nishanta Rajakaruna holds a PhD, College of the Atlantic. risks to human and ecosystem health (Ensley 2000; J. E. Gall : N. Rajakaruna (*) Sánchez 2008; Wuana and Okieimen 2011). While College of the Atlantic, 105 Eden Street, Bar Harbor, ME many heavy metals are naturally present in the Earth’s 04609, USA crust and atmosphere, humans may promote heavy met- e-mail: [email protected] al pollution through activities such as mining, smelting, R. S. Boyd transportation, military operations, and industrial Department of Biological Sciences, Auburn University, manufacturing, as well as applying metal-containing Auburn, AL 36849, USA pesticides and fertilizers in commercial agriculture. These activities release metals into the environment N. Rajakaruna Unit for Environmental Sciences and Management, through waste disposal, runoff, and application of heavy North-West University, Potchefstroom, South Africa metal-laden chemical products, which then may enter terrestrial systems via aerial deposition, surface waters, physiologically distinct taxa, metal-tolerant and metal- or soil (Järup 2003;Boyd2004 ; Pilon-Smits 2005; accumulating plants (i.e., metallophytes) and microbes Chaffai and Koyama 2011). Unlike their organic pollut- have attracted much attention, providing insights into ant counterparts, heavy metals cannot be degraded. As a adaptation (Yang et al. 2005; Haferburg and Kothe result, heavy metals persist in the environment for years, 2007;Gadd2010 ) and speciation (Ernst 2006;O’Dell well after point sources of pollution have been removed and Rajakaruna 2011)aswellasleading to the devel- (Babin-Fenske and Anand 2011). opment of certain green technologies, including Categorized into essential and non-essential groups, phytoremediation and phytomining (Chaney et al. heavy metals may interact directly with biomolecules, 2007; Wenzel 2009; Meier et al. 2012). disrupting critical biological processes and resulting in toxicity. Essential heavy metals (i.e., micronutrients), including copper (Cu), iron (Fe), manganese (Mn), nick- Microbes el (Ni), and zinc (Zn), are required by organisms in small amounts (Epstein and Bloom 2004;Marschner2012 ). Soil microbes have geoactive roles in the biosphere and Although organisms are generally able to regulate small are responsible for element biotransformations, biogeo- amounts of essential metals, in excess these metals may chemical cycling, metal and mineral transformations, become toxic (Kabata-Pendias and Pendias 2001; decomposition, bioweathering, and the formation of soil Chaffai and Koyama 2011). Contrastingly, non- and sediments (Brussaard 1997; Haferburg and Kothe essential metals such as aluminum (Al), arsenic (As), 2007; Gadd 2010). Among these important roles, mi- cadmium (Cd), lead (Pb), and mercury (Hg) are not crobes mineralize biocompounds, especially biopoly- required for normal biological function and may quickly mers like lignocellulose and chitin, by decomposing lead to toxicity (see references within Boyd and them (Haferburg and Kothe 2007). These microbial Rajakaruna 2013). Both classes of metals may accumu- roles in biogeochemical processes and elemental cycles late in tissues with potential to transfer to higher trophic are summarizedbyGadd(2010). levels (Peterson et al. 2003; Gall and Rajakaruna 2013; Although microbes have such important roles in the Neilson and Rajakaruna 2014; Bourioug et al. 2015). soil, the presence of heavy metals in soils can negatively While many studies of heavy metals focus on metal affect microbe-mediated soil processes (Lee et al. 2002). accumulation in individual taxa (e.g., Smith and Some heavy metals, such as Cu, Co, Fe, Mg, Mn, Ni, Rongstad 1982; Mesjasz-Przybylowicz and and Zn, are essential micronutrients for microbes be- Przybylowicz 2001; Miranda et al. 2009; Kupper and cause they are involved in regulating osmotic pressure, Leitenmaier 2011), fewer studies examine community- play a role in redox processes that stabilize molecules level effects (Peterson et al. 2003;Boydet al. 2006 ; through electrostatic interactions, and are key compo- Bourioug et al. 2015) of heavy metals, including their nents of certain enzymes (Gadd 2010; Boshoff et al. ability to transfer through a food chain (Goodyear and 2014). While microbes can tolerate larger quantities of McNeill 1999;Gray2002 ; Langdon et al. 2003;Mann these essential heavy metals, in excess both essential et al. 2011) and bioaccumulate in higher trophic levels. and non-essential heavy metals (e.g., Al, As, Cd, Hg, In this review, we discuss the literature on heavy metal Pb) can adversely affect microbial communities (Gadd transfer in terrestrial systems at each stage of a food 2010). In general, heavy metals reduce the amount of web, including sources of heavy metals in the environ- soil microbial biomass (SMB) and lower enzyme activ- ment. We begin with studies of metal transfer from soils ity (Gadd 1990; Chander et al. 1995; Giller et al. 1998), to microbes and producers (i.e., plants) and then discuss which, in turn, decrease diversity in soil ecosystems and metal uptake and transfer in invertebrates, small ani- change microbial structure (Bååth 1989; Giller et al. mals, and large mammals (Fig. 1). Finally, we assess 1998; Pennanen et al. 1998; Giller et al. 2009). the risk of metal accumulation in humans. We also Furthermore, when microbes are adversely affected, soil discuss some unique players along the way: plants, organic matter decomposes more slowly and soil respi- animals, and microorganisms that evade toxic effects ration decreases (Giller et al. 2009). Such toxic effects because they have adaptations that allow them to ex- may occur from natural geochemical events, but are clude, tolerate, or even accumulate high concentrations more often associated with anthropogenic metal con- of heavy metals in their tissues. Among such tamination (Gadd 2010). However, these toxic effects Fig. 1 Pathways of metal transfer in the terrestrial food web and (C3)Reglero et al.(2009); Phillips and Tudoreanu (2011); select references for each pathway (A1–G). (A1)Galland Roggeman et al. (2013); (C4) Cao et al. (2010); Sahoo and Kim Rajakaruna (2013); Van der Ent et al. (2013); Pollard et al. (2013); Street (2012); (D1) Peterson et al. (2003); Green et al. (2014); (A2) Giller et al. (2009); Gadd (2010); Boshoff et al. (2010); Cheruiyot et al. (2013); (D2) Sánchez-Chardi et al. (2014); (A3) Heikens et al. (2001); Hobbelen et al. (2006); (B) (2007b); Moriarty et al. (2012); Drouhot et al. (2014); (D3) Wenzel (2009);Holetal.(2010); Kothe and Bchel (2014); (C1) Reglero et al. (2009); (F) Chary et al. (2008); (G) Luo et al. Janssens et al. (2009); Migula et al. (2011); Nica et al. (2012); (2009); Atafar et al. (2010); McClellan and Halden (2010); Jiao Meindl and Ashman (2013); Bourioug et al. (2015); (C2)Lopes et al. (2012) et al (2002); Beernaert et al. (2007); Sánchez-Chardi et al. (2007a); may be ameliorated by applying organic matter or other chelate metals into a form that cannot be absorbed. amendments to soils, thereby increasing soil pH and However, other microbes (like the fungi Aspergillus decreasing the mobility of metals (Pérez-de-Mora et al. niger and Penicillium spp.) actually solubilize metals 2006; Friesl-Hanl et al. 2009). (rather than immobilize them) by releasing organic acids Both living and dead microbial biomass is capable of into the soil; these fungi have been used to leach