The Transfer of Trace Metals in The Soil-Plant-Arthropod System 2021

Science of the Total Environment 779 (2021) 146260
Contents lists available at ScienceDirect
Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv
Review
The transfer of trace metals in the soil-plant-arthropod system

Mark Tibbett a,⁎, Iain Green b, Andrew Rate c, Vinícius H. De Oliveira d, Jeanette Whitaker e
a
Department of Sustainable Land Management & Soil Research Centre, School of Agriculture Policy and Development, University of Reading, Whiteknights, RG6 6AR, UK
b
Department of Life and Environmental Sciences, Faculty of Science and Technology, Bournemouth University, Poole, Dorset BH12 5BB, UK
c
School of Agriculture and Environment, The University of Western Australia, Perth, WA 6009, Australia
d
Department of Plant Biology, Institute of Biology, University of Campinas, Campinas, Sao Paulo 13083-970, Brazil
e
UK Centre for Ecology & Hydrology, Lancaster Environment Centre, Library Avenue, Lancaster LA1 4AP, UK
H I G H L I G H T S G R A P H I C A L A B S T R A C T
• Cd, Cu, Zn and Ni are prevalent and la-

bile metal cations in food chains in ter-
restrial ecosystems.
• Current evidence on trophic transfer of
metals and its underlying mechanisms
are reviewed
• Compartment-based approach: metal
transfer via trophic pathways are con-
sidered as a series of linked compart-
ments
• Plants play a major role in regulating the
transfer of metals from soil to Arthro-
pods
• Biomagnification is not a general prop-
erty of plant-arthropod and arthropod-
arthropod systems
a r t i c l e i n f o a b s t r a c t
Article history: Essential and non-essential trace metals are capable of causing toxicity to organisms above a threshold concen-
Received 27 December 2020 tration. Extensive research has assessed the behaviour of trace metals in biological and ecological systems, but
Received in revised form 26 February 2021 has typically focused on single organisms within a trophic level and not on multi-trophic transfer through terres-
Accepted 28 February 2021
trial food chains. This reinforces the notion of metal toxicity as a closed system, failing to consider one trophic
Available online 8 March 2021
level as a pollution source to another; therefore, obscuring the full extent of ecosystem effects. Given the rela-
Editor: Charlotte Poschenrieder tively few studies on trophic transfer of metals, this review has taken a compartment-based approach, where
transfer of metals through trophic pathways is considered as a series of linked compartments (soil-plant-arthro-
pod herbivore-arthropod predator). In particular, we consider the mechanisms by which trace metals are taken
Keywords: up by organisms, the forms and transformations that can occur within the organism and the consequences for
Trace metals trace metal availability to the next trophic level. The review focuses on four of the most prevalent metal cations
Trophic transfer in soil which are labile in terrestrial food chains: Cd, Cu, Zn and Ni. Current knowledge of the processes and mech-
Ecotoxicology anisms by which these metals are transformed and moved within and between trophic levels in the soil-plant-
Mycorrhiza
arthropod system are evaluated. We demonstrate that the key factors controlling the transfer of trace metals
Food chain
through the soil-plant-arthropod system are the form and location in which the metal occurs in the lower trophic
Cadmium
Copper level and the physiological mechanisms of each organism in regulating uptake, transformation, detoxification
Zinc and transfer. The magnitude of transfer varies considerably depending on the trace metal concerned, as does
Nickel its toxicity, and we conclude that biomagnification is not a general property of plant-arthropod and arthropod-
⁎ Corresponding author.
E-mail address: [email protected] (M. Tibbett).
https://doi.org/10.1016/j.scitotenv.2021.146260
0048-9697/© 2021 Elsevier B.V. All rights reserved.
M. Tibbett, I. Green, A. Rate et al. Science of the Total Environment 779 (2021) 146260
arthropod systems. To deliver a more holistic assessment of ecosystem toxicity, integrated studies across ecosys-
tem compartments are needed to identify critical pathways that can result in secondary toxicity across terrestrial
food-chains.
© 2021 Elsevier B.V. All rights reserved.
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
2.1. Inputs of Cu, Ni, Cd and Zn to soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
2.2. Mineralogy and chemistry of metals in soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
2.2.1. General chemical properties of cadmium, copper, nickel and zinc . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
2.2.2. Metals in mineral phases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
2.2.3. Chemisorption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.2.4. Ion exchange . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.2.5. Effect of residence time on metal availability. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.3. Contemporary concepts for bioavailability of metals in soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.3.1. Bioavailability and bioaccessibility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.3.2. Methods for predicting bioavailability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
2.3.3. Modelling trace metal bioavailability in soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
2.3.4. Free ion activity model(s) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
2.3.5. Metal-supply-based or kinetic models. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
2.3.6. “Soil” versions of the biotic ligand model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
2.4. Transport and mobility of trace metals in soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
2.5. Rhizosphere soils: modification of trace metal chemistry by plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
2.6. Soil bioavailability and multi-trophic metal transfer. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
3. Terrestrial plants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
3.1. Availability of trace metals to terrestrial plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
3.2. Uptake of trace metals by terrestrial plants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
3.2.1. Mycorrhizal fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
3.2.2. Plant roots . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
3.3. Transport of trace metals in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
3.3.1. Metal distribution and sinks within the plant . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
3.4. Transformation of trace metals in plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
3.5. Plants and multi-trophic metal transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
4. Invertebrate herbivores. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
4.1. Availability of trace metals to herbivorous arthropods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
4.2. Uptake of trace metals by arthropods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
4.3. Transformations of trace metals in arthropods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
4.3.1. Sites of trace metal sequestration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
4.3.2. Export of trace metals from cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
4.3.3. Transport of trace metals within arthropods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
4.4. Regulation of trace metals by cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
4.5. Output of trace metals from arthropods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
4.6. Herbivorous arthropods and multi-trophic metal transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
5. Predatory arthropods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
5.1. Uptake, availability, transport, transformation and output of trace metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
5.2. Predatory arthropods and multi-trophic metal transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
6. Metal accumulation across trophic levels . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
6.1. Accumulation strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
6.2. Multitrophic transfer and biomagnification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
Declaration of competing interest. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
1. Introduction in marine diatoms (Lane and Morel, 2000; Xu et al., 2008). Both essen-
tial and non-essential trace metals are capable of causing toxicity above
Trace metals in soils (metallic elements with typical concentrations a certain threshold concentration. Extensive research has assessed the
of <1000 mg kg−1) can be divided into two groups based on their bio- behaviour of trace metals in biological and ecological systems (e.g.
logical function. The first group of elements, including Cu, Zn and Ni, are Kabata-Pendias, 2010; Adriano, 2001; Peralta-Videa et al., 2009;
essential for the correct functioning of organisms (Marschner, 2012). Hooda, 2010; Alloway, 2012a; Jan et al., 2015). However, much of this
The second group of trace elements have no known function in biolog- research has typically focused on single organisms within a trophic
ical systems (Kabata-Pendias, 2010; Alloway, 2012a). Cadmium belongs level and not on multi-trophic transfer through terrestrial food chains,
to the second group when considering terrestrial ecosystems (Smolders despite some notable field research and reviews on this topic (Fritsch
and Mertens, 2012), although a biological role for Cd has been reported et al., 2012; Nica et al., 2012; Orlowski et al., 2019; Pilon-Smits, 2019).
2
This reinforces the notion of metal toxicity as a closed system, failing to the higher compartment, and more than one such contiguous concen-
consider one trophic level as a pollution source to another; therefore, trating transfer forms a critical pathway (van Straalen and Ernst,
obscuring the full extent of its ecosystem effects. This holistic eco(sys- 1991) (Fig. 2).
tem)toxicity concept needs addressing, and is the fundamental precept The overall aim of the review is to identify the key factors controlling
for this review, which we hope will underpin more integrated research the transfer and toxicity of trace metals in excess in the soil-plant-
efforts in the future. arthropod system by addressing four research questions:
In this review we address this knowledge gap, synthesising evidence
on trophic transfers of metals and the underlying mechanisms in soil- 1. What determines the soil bioavailability of trace metals to plants?
plant-arthropod food-chains for four of the most prevalent and labile 2. What are the physiological mechanisms that regulate uptake, trans-
metal cations in terrestrial food chains (Cd, Cu, Zn and Ni). Only one pre- formation, accumulation and detoxification in plants and herbivo-
vious review has considered metal transfers in terrestrial multi-trophic rous and predatory Arthropods?
systems (Gall et al., 2015), but the authors took a much broader ap- 3. How do interactions between soil, plants and arthropods determine
proach than we apply here, in terms of the number of metals and mam- the magnitude of transfer between trophic levels?
malian and human endpoints, and did not focus on the underpinning 4. How important is biomagnification in soil-plant-arthropod systems
mechanisms. Given the relatively few studies that deal with the trophic and what are the consequences where it occurs?
transfer of metals and the large number of studies within each trophic
level, this review has taken a compartment-based approach, where 2. Soils
transfer of metals through trophic pathways is considered as a series
of linked compartments (soil-plant-arthropod herbivore-arthropod Potentially toxic trace elements are naturally present in soils,
predator). In each compartment we consider the input to the compart- being residual to a lesser or greater extent from the parent material
ment, transport and transformations that occur in that compartment and other natural sources (e.g. volcano, wind dust, forest fires)
and its transfer to the next (higher trophic) compartment (Fig. 1). (Oorts, 2012). Significant additions of some trace elements, includ-
The mechanisms by which trace metals are taken up by organisms, ing Cu, Ni, Cd and Zn have been made to many soils as a result of
the forms and transformations that can occur within the organism and human activities, from common agricultural practices to direct in-
the effect that this may have on trace metal availability to the next tro- dustrial waste disposal (Alloway, 2012b). Since potentially toxic
phic level are also explored. trace elements may be transferred through food webs, primarily as
Metals are inevitably transferred from one lower (trophic) compart- a result of plant uptake, there has been considerable attention de-
ment to the next higher (tropic) compartment but the magnitude of voted to the effect of trace element pollution in soils on the function-
transfer varies due to a complex interaction of chemical and physiolog- ing of ecosystem components and the consequent risks to human
ical factors. The net effect of these factors can be expressed as health. The behaviour of trace elements in soils, however, is complex
biomagnification (bioaccumulation) factors or transfer coefficients. and, despite considerable recent advances, there is still no unifying
Transfer coefficients (TCs) are calculated by dividing the concentration theory able to predict trace element bioavailability from soil sources.
in one compartment of the system by the concentration in the compart- Here we examine inputs and redistribution of the potentially toxic
ment below it (e.g. concentration in the arthropod divided by the con- trace elements Cu, Ni, Cd and Zn in soils, and the chemical reactions
centration in the plant tissue) (Green et al., 2003; Green and Tibbett, controlling their distribution among solid- and aqueous-phase
2008; Li et al., 2018). A transfer coefficient of less than one leads to chemical species. We conclude with an analysis of current models
the dilution of metal(s) in the higher compartment, and more than which predict actual bioavailability, or chemical proxies of this elu-
one such contiguous diluting transfer forms a benign pathway (Fig. 2). sive concept, as tools that can be applied in research focused on
A coefficient greater than one leads to the concentration of metals in metal transfer across trophic levels.
Fig. 1. Conceptual compartmentalised model system for transfer of metals in a linear pathway from basal abiotic (soil) sources to higher biotic trophic levels in the soil-plant-arthropod
system. Red circles represent metals and numbers 1 to 4 represent a trophic compartment.
3
Fig. 2. Model compartment systems representing (a) benign (transfer coefficient < 1) and (b) critical (transfer coefficient > 1) pathways for dilution or concentration of metals in the soil-
plant-arthropod system.
2.1. Inputs of Cu, Ni, Cd and Zn to soils (Kopittke et al., 2017), or TOF-SIMS (Time of flight secondary ion mass
spectrometry; Arenas-Lago et al., 2016). Determination of soluble
Trace elements occur naturally in the parent materials of soils, at metals remains complicated by the difficulties in separating truly aque-
concentrations which are broadly dependent on lithology. During the ous species from dispersed colloids. Techniques which target a concep-
process of soil formation, trace elements become enriched or depleted tual fraction rather than a discrete species may, in fact, be more useful in
in different soil horizons. This depends on the soil-forming environment predicting biological uptake than true speciation methods (McLaughlin
and the predominant chemical reactions for each element (Adriano, et al., 2000; Zhang et al., 2001a, b; Van der Ent et al., 2019).
2001), for example, soil weathering and clay enrichment are associated
with higher background levels of Zn (Mertens and Smolders, 2012). 2.2.1. General chemical properties of cadmium, copper, nickel and zinc
External inputs of trace elements include atmospheric deposition, The chemical occurrence and reactions of Cd, Cu, Ni and Zn in natural
such as from wind-blown dust, forest fires and volcanic ashes environments have been reviewed thoroughly by several authors. The
(Alloway, 2012b; Oorts, 2012), which is minimal in many natural following is a brief summary of the significant chemical properties for
environments (e.g., Gray et al., 2003) but may be locally important. these elements; (for more detail, we refer the reader to Adriano, 2001
Summaries of average concentrations of trace elements in different and Alloway, 2012a). All four elements exist predominantly as divalent
rock types have been presented by Kabata-Pendias (2010), Alloway cations in natural systems (Cu0 and Cu+ may exist under some redox
(2012b) and Adriano (2001). conditions, but are uncommon). The aqueous speciation of Cd2+,
Anthropogenic activity has elevated concentrations of Cu, Ni, Cd and Cu2+, Ni2+ and Zn 2+ is mostly as stable complexes or ion pairs, as
Zn in soils across the globe and most research into trace metal bioavail- well as aquo-complexes and their hydrolysis products. The divalent
ability has focused on such environments. Anthropogenic sources of cadmium ion is a soft Lewis acid, and shows a preference for reduced
trace metals have been reviewed exhaustively (e.g., Kabata-Pendias, sulphur, some N-donor, or halide ligands. Divalent Cu2+, Ni2+ and
2010; Adriano, 2001; Naja and Volesky, 2009; Alloway, 2012b). Indus- Zn2+ are intermediate Lewis acids and form ion pairs or complexes
trial inputs include mining and ore processing, smelting and other met- with a range of ligands, many with O- or N-containing functional
allurgical processes and a wide range of metal-utilizing industries. groups, including sulfate, chloride and numerous organic ligands such
Agricultural activities contributing metals include use of fertilizers as simple carboxylates and natural dissolved organic matter. All four el-
with trace element supplements or impurities, application of metal- ements form insoluble hydroxides, carbonates, phosphates and sulfides.
contaminated organic wastes including sewage sludge or effluents A co-occurrence of Cd and Zn is often reported for both contaminated
from animal industries, and use of metal-containing pesticides, espe- (Anju and Banerjee, 2011) and non-contaminated soils (De Oliveira
cially Cu and Zn in fungicides. Enhanced atmospheric deposition has et al., 2014), but a large meta-analysis did not find this to be the case
also resulted from use and disposal of fossil fuels and their residues. for a wide range of soils globally (Hamon et al., 2004).
2.2. Mineralogy and chemistry of metals in soils 2.2.2. Metals in mineral phases
Many trace elements including Cu, Ni, Cd and Zn occur as discrete
Trace elements are present in a range of chemical forms in soils. mineral phases containing the element of interest as the primary struc-
These may be inherited from unaltered parent material; alternatively, tural cation (such as hydroxides, carbonates, phosphates and sulfides),
metal speciation in soil may reflect a combination of pedogenetic trans- or as ions co-precipitated in variable proportions in the structure of
formations and/or anthropogenic additions. It is unquestionable that more common minerals such as primary and secondary silicates, and
the form of trace elements is a major control on their availability or ac- oxyhydroxides of Fe, Al and Mn (Kabata-Pendias, 2010). Whilst trace
cessibility to organisms, and this has been reviewed thoroughly (Allen metals within primary or pedogenic mineral structures provide useful
et al., 2001; Basta et al., 2005; McLaughlin et al., 2000; Nolan et al., data on geochemical origins and soil-forming processes, these forms
2003; Tessier and Campbell, 1987; Antoniadis et al., 2017). However, of elements are not usually considered to contribute to biological uptake
despite the importance of metal speciation in soils, methods for accu- due to their slow cycling within terrestrial ecosystems. Exceptions to
rately determining speciation require further refinement. Total elemen- this generalisation include trace metal ions coprecipitated with second-
tal analyses, which include all forms of metals in soils, do not generally ary iron or manganese oxyhydroxides (Wang and Jia, 2017), or present
correlate well with biological uptake (McLaughlin et al., 2000; Nolan in sulfide minerals (Kabata-Pendias, 2010). Changes in soil redox poten-
et al., 2003; Kim et al., 2015). For example, the existence of metals in tial can result in transient fluxes of dissolved metal ions from these min-
specific mineral phases in soils may be established using microprobe erals via processes such as reductive dissolution of oxides, or sulfide
techniques such as EDS (having relatively high detection limits; oxidation (Gambrell, 1994; Singh et al., 1996; Rinklebe et al., 2016).
Nielsen et al., 2015), synchrotron X-ray spectroscopic techniques There is some evidence to show that, over a wide geographical range,
4
several trace elements including Cu, Ni, Cd and Zn co-occur with iron Although these correlations may occur for some elements, such as Cd,
minerals in soils (Hamon et al., 2004; De Oliveira et al., 2014). It should plant uptake of other metals (e.g. Cu, Ni and Zn) was shown to be poorly
be noted, however, that despite the predominance of metals in mineral correlated to the “easily extracted” fraction in soils determined via the
phases and their purported lack of bioavailability, correlations between CaCl2 method (Pauget et al., 2015).
total metal concentrations in soils and bioavailability as determined by Concentrations of metals in soil solution are usually very low com-
plant uptake have been observed (e.g., McGrath et al., 2000). In some pared with those in the solid phase, and reflect a combination of equilib-
cases, metals in nanoparticulate phases in soils may contribute to rium with sparingly soluble and sorbed forms of metals, and formation
enhanced bioavailability (e.g., Unrine et al., 2010; Watson et al., 2015), of soluble inorganic and organic complexes (Wolt, 1994). A critical pa-
but in several cases the nanoparticles themselves can be assimilated by rameter is the activity or concentration of “free” metal ion, the value
organisms and cause toxicity, such as observed in bacteria (Sirelkhatim of which is central to the free-ion activity model of bioavailability
et al., 2015), plants (Tripathi et al., 2017) and animals (Johnston et al., discussed below.
2010). Studies on the bioavailability, transport and toxicity of nanoparti-
cles in higher plants have been summarised in reviews from Miralles 2.2.5. Effect of residence time on metal availability
et al. (2012), Mustafa and Komatsu (2016), and Tripathi et al. (2017). Whether trace metals such as Cu, Ni, Cd or Zn enter soil as ions or as
components of amendments such as fertiliser or sewage sludge, short-
2.2.3. Chemisorption term pedological processes act to change their speciation and bioavail-
Chemisorption (adsorption by formation of electron-sharing bonds) ability (e.g., Smolders et al., 2009; Van Oort et al., 2018). Laboratory
is likely to be very important in terms of bioavailability, based on either studies (e.g., Backes et al., 1995; Qiang et al., 2017) commonly demon-
free ion activity concepts (exerting control on free ion activities) or on strate that, if metal ions react longer with soil components they desorb
kinetically based models for bioavailability (since some desorption oc- less and the desorbed fraction is released more slowly than for shorter
curs over timescales which are likely to be relevant to replenishment reaction times. A contrasting concept is the “time bomb” hypothesis,
of free ions). Chemisorption of Cd2+, Cu2+, Ni2+ and Zn2+ at the where it is thought that metals applied in organic residues such as sew-
water-particle interface occurs by surface complexation mechanisms. age sludge will increase in bioavailability in the medium- to long-term,
Such adsorption involves weakly acidic (e.g., organic –COOH) or ampho- following mineralisation of organic adsorbing phases and associated
teric (e.g., terminal –OH on phyllosilicates or sesquioxides) functional acidification (McBride, 2003; Bramryd, 2013). For example, the concen-
groups forming coordinative bonds with metal cations. Typically, sur- tration of available Cd was shown to increase in soils under pig manure
face complexation of metal ions occurs at deprotonated sites or by dis- application only after 10 years (Xu et al., 2015). McGrath et al., (2000),
placement of H+, so the reactions are favoured at high pH (Sposito, however, found that Zn and Cd extractability from soil did not change
1989). Chemisorbed trace metal cations in soils are most likely those significantly >20 years following sewage sludge application, results
targeted by common wet chemical extraction methods (e.g., DTPA ex- which do not support either increased or decreased bioavailability in
traction, acetate buffer; Zhang et al., 2010). Chemisorption is commonly the long-term. Some steps towards resolution of this issue have been
considered to show poor “reversibility”, deduced from observations of made by Bergkvist and Jarvis (2004), who show by a modelling ap-
desorption hysteresis (McLaren et al., 1981; Shaheen et al., 2013). The proach that long-term changes in metal bioavailability vary according
apparent lack of reversibility most likely reflects experimental factors; to soil and sewage sludge properties and metal content, and that no uni-
insufficient time for the forward reaction means that equilibrium is versal outcomes exist.
not achieved, and the difference in apparent equilibrium for the subse-
quent desorption phase is a consequence of the longer time elapsed. In 2.3. Contemporary concepts for bioavailability of metals in soils
some cases this may mean that rapid, strong adsorption is a metastable
state, effectively a precursor for coprecipitation or physically/sterically 2.3.1. Bioavailability and bioaccessibility
constrained adsorption (e.g., Rate et al., 1993; McLaren et al., 1998). It is significant that there is still some contention about how bioavail-
ability should be defined for soil systems; many studies and reviews
2.2.4. Ion exchange contain implicit operational definitions, or avoid making a definition al-
The occurrence of Cd2+, Cu2+, Ni2+ and Zn2+ as cations means that together (e.g., Basta et al., 2005; Nolan et al., 2003; Antoniadis et al.,
they can be retained by electrostatic sorption (i.e., ion exchange) on neg- 2017). Semple et al. (2004) distinguish bioaccessibility and bioavailabil-
atively charged soil colloids such as phyllosilicates and organic matter. ity, where a substance is bioavailable if a transfer from soil into an organ-
Since variable charge is more negative at high pH, the capacity of soils ism can occur, and bioaccessible substances are able to resupply the
to hold cations electrostatically increases as pH increases (Antoniadis bioavailable pool, but are separated from organisms spatially or tempo-
et al., 2017). The exchangeable fraction of metals usually represents a rally, depending on their chemical or physical state. A common and
low proportion of total metal content in soils. Lower concentrations of often implicit assumption is of a continuum of “bioavailability” decreas-
exchangeable trace metals reflect the unfavourable thermodynamics of ing from free ions in solution to exchangeable ions, chemisorbed ions,
electrostatic sorption compared with other mechanisms, and competi- and finally ions within mineral structures. In summary, bioavailability
tion at charged particle–water interfaces by high concentrations of di- refers to a chemically active compound readily available to an organism,
or trivalent major cations (Ca2+, Mg2+, and Al3+). Sorption reactions whereas bioaccessibility refers to a chemically inactive but potentially
in soils can be considered to effectively form a continuum with respect exploitable compound (Semple et al., 2007; Kim et al., 2015). Such dis-
to affinity for metal cations at concentrations at which high affinity crimination is particularly interesting for bioremediation studies, in
chemisorption ‘sites’ are fully occupied by metal ions, therefore, lower- which the bioaccessible fraction can be a useful endpoint for assessment.
affinity sites then become more important for metal ion retention. As a
result, in contaminated soils, compared with uncontaminated, there 2.3.2. Methods for predicting bioavailability
may be a higher proportion of weakly-bound metal ions, some of It can be assumed, simplistically, that measurable fractions of metals
which may be held in ion-exchangeable form. Again, some wet chemical in soils represent the bioavailable and/or bioaccessible component,
extraction methods (e.g., 0.01 M CaCl2; Whitten and Ritchie (1991); Van without explicitly considering the biological uptake mechanism. This
der Ent et al. (2019) and review by McLaughlin et al. (2000)) appear to provides the rationale behind numerous chemical extraction techniques
be designed to selectively determine trace metal cations in this fraction. for measuring a fraction of metals in soils, using electrolytes, dilute acids
The success of some of these methods, in determining fractions of metals and/or buffers, or complexing agents, including many sequential extrac-
which correlate well with plant uptake, may reflect the importance of tion schemes (Lindsay and Norvell, 1978; Shuman, 1985; Tessier et al.,
weakly-sorbed exchangeable ions as a buffer for the soil solution pool. 1979; Whitten and Ritchie, 1991). Further efforts, to improve the ability
5
to predict bioavailability, have assumed that using an extractant which toxicity and uptake in Hordeum vulgare growing in soil, even when
simulates the composition of earthworm gut fluids (e.g., relevant en- plants were exposed to a mixture of both metals; despite not accounting
zymes, anoxia) will more accurately reflect uptake and toxicity (Ma for internal transport mechanisms.
et al., 2009). Smith et al. (2010) showed that Cu, Pb and Zn extracted
by a simulated earthworm gut extractant were correlated with some 2.3.5. Metal-supply-based or kinetic models
toxicity outcomes for plants, earthworms and collembolans in soils, Compelling evidence that metal ion uptake by plants is a function of
out-performing total metal and other extractable metal concentrations. both instantaneous dissolved concentration and the kinetics of resupply
Using soil metal concentrations in combination with other soil chemical from soil solid phases comes from the work of Davison et al., 1999 and
data has also been employed to predict metal bioavailability. A promis- Zhang et al. (2001a, b). The study by Zhang et al. (2001a, b) showed that
ing approach was presented by McBride et al. (1997), who proposed a the “effective concentration” of Cu (CE) measured by diffusive gradients
semi-mechanistic model using total analyses of metals in soils in combi- in thin films (DGT), was the best predictor of copper uptake by plants,
nation with measurements of soil parameters known to influence metal followed by (in order) total dissolved Cu, free Cu2+ activity, and Cu ex-
ion speciation (pH, organic carbon content) to successfully predict con- tracted with EDTA solution. This confirms work showing that isotopi-
centrations of metals in soil solution. More recent work by Smolders cally exchangeable metal ions correlate well with metal uptake by
et al. (2009) showed that the best predictor of toxicity thresholds to plants (Hamon et al., 2002) and also older work showing plant uptake
plants or invertebrates (earthworms or collembolans), over a large correlating with exchangeable 〈or neutral electrolyte-extractable〉
range of soils, was the total concentration of metal in soil as a proportion metal ions with relatively short extraction times (e.g., Whitten and
of effective (unbuffered) cation exchange capacity (ECEC). This ratio Ritchie (1991); and discussed in the review by McLaughlin et al.
needed to be corrected for leaching and/or aging of contaminated soils (2000)). Several subsequent studies have confirmed the ability of DGT
in the field, and the study also showed that neither soil pH nor free to predict phytoavailability under some soil conditions (e.g. (Mason
metal ion activity could reliably predict toxicity endpoints (Smolders et al., 2010; Perez and Anderson, 2009; Puschenreiter et al., 2013), but
et al., 2009). Nevertheless, Pauget et al. (2012), studying trace metals other studies do not show any relationship between metal ion fluxes
in snails, concluded that a good prediction of environmental bioavail- measured by DGT and plant uptake. Oporto et al. (2009) show that at
ability may come from focusing on total soil concentrations coupled high soil Cd supply, where diffusion to the organism surface may not
with the influence of soil characteristics, such as pH and CEC. When con- be limiting, DGT is not a good predictor of plant Cd uptake. In a study fo-
sidering both snails and plants, the accumulation of metals were influ- cusing on toxicity thresholds rather than uptake, Smolders et al. (2009)
enced by very different parameters, mostly due to their physiological also showed that DGT could not predict Zn toxicity endpoints (EC50)
mechanisms (e.g. rhizospheric processes) and acquisition sources, i.e. across a range of soils; the focus on toxicity presupposes that the
superficial/deep soil layers for plants, and superficial soil and plant ma- range of soil Zn concentrations also reached high values. In contrast,
terial for snails (Pauget et al., 2015). Thus, the authors concluded that Tandy et al. (2011) tested the prediction capacity of DGT for plant-
bioindicators should complement chemical procedures to get better in- available Cu and Zn in several soil types and at agronomical relevant
sights into contaminated areas. concentrations, and found this method to be more accurate than the
A consensus has now emerged that bioavailability is a process that usual EDTA and DTPA methods. Two reviews (Degryse et al., 2009;
cannot be attributed to one single value, measured by a single method. Zhang and Davison, 2015) analysed a number of studies relating DGT
There is a plethora of chemical techniques and biological systems de- metal analyses in soil to bioavailability. Both works concluded that
vised for accessing trace metal bioavailability, such as invertebrate, DGT can validly predict plant uptake in situation where diffusion of
plant and microbial tests – including single cell biosensors – which metal ions to plant roots is limiting, but not where soil metal concentra-
can measure different endpoints (toxicity, enzymatic activity, antioxi- tions are high (in agreement with Oporto et al. (2009) and Smolders
dant compounds, fluorescence, bioluminescence etc.). Such methods et al. (2009)). Labile metal complexes also contribute to DGT assays,
have been thoroughly reviewed by Kumpiene et al. (2017). and such complexes may or may not be taken up by plants (Degryse
et al., 2009).
2.3.3. Modelling trace metal bioavailability in soils
Metal availability in soils is the initial step from which a contaminant 2.3.6. “Soil” versions of the biotic ligand model
enters the food chain and moves up trophic levels. Therefore, models that The biotic ligand model extends chemical equilibrium modelling to
can effectively predict trace metal bioavailability in soil and plant uptake include the biological receptors on an organism as additional ligands
are the foundation for understanding transfer of trace metals in the soil- for which complexation is competitive, as for other ligands, between
plant-arthropod system and for ecotoxicological risk assessments. metal ions and protons (Di Toro et al., 2001; Slaveykova and Wilkinson,
2005) (Fig. 3; see later section on uptake by plant roots). A distinguishing
2.3.4. Free ion activity model(s) feature of the biotic ligand approach is that metal ion toxicity is not af-
The free-ion activity model of bioavailability assumes that metal up- fected by chemical gradients in the bulk solution (e.g. concentrations,
take will be proportional to the activity of the free, uncomplexed metal pH), and its predictions depend on the amount of metal effectively
ion in solution (Parker and Pedler, 1997). Whilst some studies have bound to biological receptors, therefore toxic effects are less likely at
shown a positive relationship between metal ion activity and plant up- lower pH, where other available metals (such as Ca2+ and Co2+) will
take (Nolan et al., 2005; Van Gestel and Koolhaas, 2004; Zhang et al., compete for the same biological carriers (Wang and Song, 2019). The bi-
2001a, b; Shahid et al., 2011; Qiu and He, 2017), the free ion activity otic ligand model (BLM) has successfully predicted bioaccumulation and
model does not account for resupply from soil solid phases which buffer toxicity to fish and other aquatic organisms (Nolan et al., 2003; Blewett
metal ion activities, nor does it explicitly consider competition at the and Leonard, 2017). Weng et al. (2003), however, suggested that the
solution–organism interface or the influence of plant metabolism in magnitude of soil effects may overwhelm biotic ligand effects for Ni up-
the rhizosphere, and therefore would not necessarily be expected to take; their work showed that the effect of pH follows that expected, if
apply in soils (Parker and Pedler, 1997; Parker et al., 2001). For instance, dissolved Ni2+ activity is controlled via adsorption or precipitation rather
predicted free ion activities failed to explain metal concentrations in than competition for a biotic ligand. Conversely, a study by Van Gestel
snails from soils contaminated by Cd, Pb and Zn, whilst a better predic- and Koolhaas (2004), of Cd accumulation by collembolans, presented
tion was obtained when total metal concentrations and soil variables data to suggest that a BLM approach may be applicable for bioavailability
were used as explanatory variables (Mourier et al., 2011). However, a in soil.
recent model for ‘free metal ion activity at the plant cell membrane’ de- Thakali et al. (2006) showed that a terrestrial BLM predicts toxicity
veloped by Qiu and He (2017) accurately predicted Cu2+ and Zn2+ of soil-derived Cu2+ and Ni2+ to plants, such that root elongation
6
amount and type of adsorbing phases, pH, Eh) consequently affect

metal transport, as do formation of soluble complexes or adsorption
on mobile colloids. The intensity of sorption reactions in soils decreases
in the approximate order Cu > Zn ≈ Ni > Cd (e.g., Baker and Senft,
1995; Adriano, 2001; Young, 2012), with mobility increasing in the
same order, but this ranking can vary with soil characteristics and is
not replicated in all studies. Even for relatively weakly adsorbed ele-
ments like Cd, mobility is often observed to be low. The resulting
small transport distances over observable time scales are shown by
the retention of contaminant-derived metals in surface soil horizons,
except in very acidic or sandy soils (Adriano, 2001). Over longer time-
scales, highly leached soils such as podzols show evidence of metal mo-
bility in the form of near-surface depletion and enrichment in subsoil
horizons (e.g., Berggren, 1992). Mass transport of metal ions is likely
to be dominated by preferential water flow, which is influenced by
soil texture and structure (McLaren et al., 2004; Tack, 2010), with in-
creasing recognition of colloid transport as a mechanism enhancing
mass fluxes of metals (Sherene, 2010; Won et al., 2019). If the implica-
tions derived from use of the DGT technique (Zhang et al., 2001; Zhang
and Davison, 2015) are valid, however, metal ion supply to plants seems
more likely to occur by diffusion than mass transport. Diffusive transport
depends on the concentration gradient, ionic diffusion coefficient and
physical factors, such as water film thickness (Sparks, 1989; Carrillo-
Fig. 3. Conceptual diagram showing the interactions considered in the terrestrial biotic
ligand model for metal ions (M2+).
González et al., 2006). The plant root's ability to minimise diffusion dis-
(From Thakali et al., 2006). tances is therefore critical, and this is discussed in later sections.
2.5. Rhizosphere soils: modification of trace metal chemistry by plants

could be predicted from the amount of Cu2+ or Ni2+ bound to a biotic
ligand, whilst Lin et al. (2018) also predicted Cu toxicity effectively Plants have various strategies for modifying the uptake of trace
with BLM, in which H+, Ca2+ and Mg2+ were shown to alleviate its tox- elements such as Cd, Cu, Ni or Zn from soil in the immediate vicinity
icity. The BLM-based approach was also efficient in combined toxicity of of roots. Lowering of rhizosphere pH by H+ release affects solubility
Cu and Zn nutrient solution, also inversely correlated to Ca2+ and Mg2+ and chemisorption equilibria, increasing soil solution concentrations
concentrations (Wang et al., 2017a, b), whilst an adaptation of the BLM, of trace metal cations which are then susceptible to plant uptake
for nonlinear metal relationships was successfully used to predict allevi- (Marschner et al., 1986; Gomes et al., 2016). Production of metal-
ation effects of Ca2+, Mg2+ and K+ in Cd+2 toxicity in Glycine max roots complexing ligands by plants also increases metal concentrations in
(Chen et al., 2017). The predictive ability of these models, however, was solution, perturbing sorption and solubility equilibria as complexation
restricted to the conditions of their study, which included a high range reactions lower free metal ion activity (Merckx et al., 1986). Some
of total metal ion concentrations, to reflect the focus on toxicity and metal-organic complexes have been shown, in solution culture, to be
contaminated soils. Whether the terrestrial BLM approach would pre- bioavailable for Cd (Cabrera et al., 1988) and Cu (Guo et al., 2008), as
dict metal ion uptake in uncontaminated soils is not yet determined. have been some complexes with simple inorganic ligands (Smolders
The BLM approach implicitly assumes equilibrium, and in many cases and McLaughlin, 1996). Phytosiderophores (PS) released into the rhizo-
metal ion bioavailability is likely to be controlled by rate-of-supply, sphere are also able to form PS-metal complexes and increase the bio-
with kinetics limited by diffusion or rate of release from a solid phase; availability and uptake of Cu, Ni and Zn (Puschenreiter et al., 2017),
this may be the reason for the success of DGT in predicting plant uptake however, the strength of binding and the capacity of roots to take up
in some studies (e.g., Zhang et al., 2001; Zhao et al., 2006; Perez and PS-metal complexes appears to vary among these metals (Kudo et al.,
Anderson, 2009; Ahumada et al., 2014). Interestingly, the BLM approach 2007). Even though oxidation/reduction reactions in the rhizosphere
predicts phytotoxicity under the conditions (high soil metal contents) are largely influenced by microbial activities (Seshadri et al., 2015; Ma
where DGT predictions have been shown to fail (Oporto et al., 2009). et al., 2016), lowering of the redox potential of the rhizosphere is
Nevertheless, models such as the BLM need constant refining and exploited by some plants as a mechanism for enhancing Fe and Mn up-
calibration, an example is inclundig metal toxicokinetics (TK) into the take by reductive dissolution of FeIII or MnIV oxyhydroxides (Marschner
equation, considering uptake/elimination rates and internal distribution et al., 1986), but it is unclear whether this mechanism also affects up-
(highly variable among different organisms), which may lead to a more take of associated trace elements such as Cd, Cu, Ni or Zn. Plants growing
predictive capability for metal bioaccumulation and toxicity (Ardestani in anoxic soils can also add oxygen to their rhizosphere via aerenchyma,
et al., 2014). which can oxidise and dissolve sulfides and associated trace elements
(Du Laing et al., 2009). Rhizosphere oxidation is also known to deposit
2.4. Transport and mobility of trace metals in soils ferric oxyhydroxides (“iron plaque”) adjacent to roots (Begg et al.,
1994), a process which co-accumulates trace elements such as Zn. As
Transport phenomena for trace elements in soils have been for rhizosphere reduction, however, the significance of rhizosphere ox-
reviewed thoroughly by Carrillo-González et al. (2006). Generally, mo- idation for elements other than Fe and Mn is unclear (Du Laing et al.,
bility of Cd, Cu, Ni and Zn is low relative to the rate of water movement 2009), although new findings suggest that aerobic conditions tend to re-
in soils. This low mobility is a consequence of reactions which partition lease Cd, Cu and Pb in soils (Rinklebe et al., 2016).
metal ions into solid phases: (co)precipitation; adsorption; and ion ex-
change. The thermodynamics of these reactions favour the existence of 2.6. Soil bioavailability and multi-trophic metal transfer
metals in solid phases, and the low observed mobilities also suggest that
rates of metal ion release to the aqueous phase are slow. Factors which The bioavailability of trace elements such as Cd, Cu, Ni and Zn in soil
affect these equilibria (mainly metal ion identity and concentration, is a complex issue and, despite considerable progress being made, there
7
are clearly ongoing issues with defining a bioavailability concept in soils Bever et al., 2010). However, their contribution to nutrient uptake is
and understanding the purely soil-related factors which affect the trans- particularly important for those nutrients that are diffusion limited
fer of trace elements to organisms. The following discussion is informed due to their low mobility in soils, including P, Cu and Zn. For example,
by the basic soil chemical concepts described in the preceding sections, in Trifolium repens, 50–60% of total Cu and Zn uptake was provided by
augmented by advances in understanding of the role of chemical and AM hyphae (Li et al., 1991), and in Solanum lycopersicum 24% of Zn
physical kinetics, and in the ability of organisms themselves to modify was delivered by the same pathway (Watts-Williams et al., 2015). Stud-
trace element behaviour in soils by extracellular phenomena. A knowl- ies also show that the majority of Cu and Zn taken up by AM fungi is
edge of soil processes alone cannot address within-organism transfers; retained in the roots, although increased translocation to the shoots
the following section, therefore, focuses on the response of plants to has also been recorded (Lee and George, 2005; Garg and Aggarwal,
the conditions created by soil processes, and the internal processes of 2012; Zheng et al., 2015). For Cd and Ni evidence on the influence of
the plants. AM colonisation on uptake is contradictory. In Phaseolus vulgaris, Zea
mays, Phleum pratense and Trifolium subterraneum AM symbiosis was
3. Terrestrial plants shown to increase uptake of Cd2+ with the majority of the Cd being
retained in the roots (Arnold and Kapustka, 1993; Guo et al., 1996;
Terrestrial plants have developed a range of mechanisms to assimi- Joner and Leyval, 1997). In contrast, in cucumber plants AM infection
late trace metals from soil environments with widely differing physical decreased concentrations of Cd in both the roots and shoots (Lee and
and chemical characteristics. In this section we discuss the plant physi- George, 2005); similar results were also found in pigeonpea (Garg and
ological processes that govern the uptake, transport, transformation and Chandel, 2012), maize (Liu et al., 2014) and for both Zn and Cd in
storage of metals in plant tissues. These include the influence of roots hyperaccumulator Thlaspi praecox (Vogel-Mikuš et al., 2006). With re-
and their associated mycorrhizal fungi on metal availability in the rhizo- spect to Ni uptake by AM fungi there have been very few studies per-
sphere, and the factors regulating transport, complexation and seques- formed with divergent results. For instance, AM infection reduced Ni
tration of metals within the plant. All these processes affect the concentrations in the roots and shoots of at least six plant species stud-
distribution and concentrations of trace metals throughout the plant ied, typically by increasing biomass production (Guo et al., 1996; Lee
and consequently influence the degree of exposure of arthropods to and George, 2005; Orlowska et al., 2011; Amir et al., 2013; Shabani
trace metals. et al., 2016), whilst AM fungi enhanced Ni uptake in soybean, lentil
and sunflower plants in contaminated soils (Jamal et al., 2002; Ker
3.1. Availability of trace metals to terrestrial plants and Charest, 2010).
ECM and ERM fungi mainly colonise trees and ericaceous shrubs.
Prior to transport across the root plasmalemma a number of factors They play a key role in the mobilisation and uptake of organic and inor-
can affect trace metal availability to the plant, with the specific mecha- ganic N and P providing access to nutrient sources not directly available
nisms employed varying among plant taxa. Plant roots typically in- to plants (Tibbett and Sanders, 2002; Cairney and Meharg, 2003), and
crease the availability of metal ions to uptake proteins by acidifying are also known to mobilize trace metals by dissolving a variety of Cd,
the rhizosphere through the release of H+ or carboxylic acids (e.g. Cu and Zn-bearing minerals, including metal phosphates (Gadd et al.,
Pang et al., 2010) and consume or release O2 altering the redox poten- 2012). Plant species colonised by ECM and ERM fungi can also grow suc-
tial. In addition, the secretion of low-molecular weight compounds cessfully on highly metal-contaminated sites (Colpaert et al., 2011;
can mobilize metals directly by functioning as metal chelators, or indi- Saraswat and Rai, 2011; Wen et al., 2017). They exhibit decreased sen-
rectly by stimulating microbial activity in the rhizosphere (Marschner, sitivity to a wide range of essential and non-essential metals including
2012; Clemens, 2006; Parrotta et al., 2015). Cd, Zn, Ni and Cu, however, metal tolerance or sensitivity varies widely
A further factor affecting the availability and uptake of trace metals between plant and mycorrhizal species (Bradley et al., 1982; Bücking
by terrestrial plants is the formation of symbiotic associations between and Heyser, 1994; Chen and Tibbett, 2007; Frey et al., 2000; Gadd
the majority of plants and mycorrhizal fungi. Mycorrhizal fungi reside in et al., 2012; Hartley-Whitaker et al., 2000; Hrynkiewicz and Baum,
the rhizosphere as spores, hyphae and propagules and colonise plant 2013; Sell et al., 2005; Mrnka et al., 2012). The mechanistic basis of
roots forming a link between the plant and the rhizosphere soil. The ex- the role of ECM and ERM fungi in plant metal tolerance or decreased
ternal mycelium of these commonly mutualistic associations plays a key sensitivity is poorly understood. For ECM fungi a number of mechanisms
role in nutrient uptake of most terrestrial plants by accessing nutrients have been postulated including extracellular binding, reduced uptake,
beyond the diffusion zone of the root, and also accessing inorganic metal efflux, intracellular chelation or compartmentation in the vacu-
and organic nutrients not readily available to plants. Up to thirteen my- oles by polyphosphate granules (Hartley et al., 1997; Lanfranco, 2007;
corrhizal types have been defined, the dominant ones being: arbuscular Colpaert et al., 2011; Luo et al., 2014). In the ECM fungus Paxillus
mycorrhizas (AM), ectomycorrhizas (ECM) and ericoid mycorrhizas involutus key mechanisms proposed for Cd tolerance are the complexa-
(ERM) (Kariman et al., 2018). Each mycorrhizal type differs in its struc- tion by metallothioneins (MT) or by phenolic compounds (Jacob et al.,
tural characteristics and forms symbioses with particular groups of 2004), whilst two MT genes from Laccaria bicolor were shown to confer
plants including grasses, forbs, crop plants, shrubs, orchids and trees. tolerance to both Cd and Cu (Reddy et al., 2014). However, as results on
Their essential functions of bi-directional nutrient exchange of carbon the effects of ECM colonisation on metal uptake and localisation are so
from plant to fungus, and soil nutrients from fungus to plant are similar, varied it is likely that mechanisms used vary between plant species
with the exception of mycoheterotrophic plants (Bidartondo, 2005). and their symbionts. For ERM fungi, the shoots of ERM plants generally
contain less metal than non-mycorrhizal plants (Bradley et al., 1982). In-
3.2. Uptake of trace metals by terrestrial plants deed, Calluna vulgaris plants under ERM symbiosis were more tolerant
to Cu toxicity, and presented lower shoot Cu accumulation than the
3.2.1. Mycorrhizal fungi non-mycorrhizal plants (Gibson and Mitchell, 2006). Therefore, avoid-
In addition to altering the availability of metals to plants in the rhizo- ance or sequestration strategies are likely to contribute to the observed
sphere, mycorrhizal fungi also enhance or regulate nutrient uptake and tolerance. According to Martino et al. (2000), in the ERM fungus
transport in plants. AM hyphae colonise many agriculturally important Oidiodendron maius, mechanisms such as production of mucilage and
plants and take up nutrients such as P, N, Cu and Zn (Ryan and extracellular pigments may be pivotal in Cd and Zn tolerance. Studies fo-
Tibbett, 2008; Cavagnaro, 2008; Watts-Williams et al., 2015), and are cusing on gene expression and characterization in O. maius are being
also important in natural and semi-natural ecosystems where they carried out to explain the genetic mechanisms for Cd and Zn tolerance
have a role in structuring plant communities (Standish et al., 2007; in this species (Daghino et al., 2016; Di Vietro et al., 2014; Khouja
8
et al., 2013). These strategies would reduce the concentrations of metal small in relation to the concentration of competing ions (Clarkson and
entering the plant root/shoot, and consequently reduce exposure of ar- Lüttge, 1989) (see earlier discussion on biotic ligand model). Competi-
thropods to trace metals in contaminated soils. tive uptake of Zn2+, Cu2+, Cd2+ and Ni2+ has been reported in a
range of plants (Brar and Sekhon, 1976; Bowen, 1981, 1987; Cataldo
3.2.2. Plant roots et al., 1978, 1983). It therefore appears that multiple pathways exist
Our understanding of the entry of cations into plant cells has been ad- for most metal ions.
vanced through molecular investigations (Clemens, 2001; Kramer et al.,
2007). A number of metal transporters have been identified in Arabidopsis 3.3. Transport of trace metals in plants
thaliana and Nicotiana spp., which are involved in the uptake, transloca-
tion and sequestration of metal ions, and many of these have also been From the cells on the surface of the root, ions are transported both
studied in the metal hyperaccumulating plants, Arabidopsis halleri and symplastically and apoplastically through the root cortex to the endo-
Noccaea (Thlaspi) caerulescens (Bovet et al., 2006; Kramer et al., 2007; dermis. The endodermis then acts as a semi-permeable membrane
Broadley et al., 2007; Lochlainn et al., 2011). At the plasma membrane, across which ions can be regulated and actively transported into the
uptake of Zn2+ from the rhizosphere is mediated by metal-uptake trans- pericycle (Punz and Sieghardt, 1993). There is evidence that the mech-
porters belonging to the ZIP family (Fox and Guerinot, 1998; Clemens, anisms sequestering trace metals in the roots and/or governing the
2006; Campos et al., 2017; Zhang et al., 2017), with16 identified in loading of trace metals into the xylem fluid are important in regulating
A. thaliana (Colangelo and Guerinot, 2006). These proteins are ubiquitous the translocation of trace metals from the root to the shoot (Hart et al.,
in eukaryotes and transport Zn from the extracellular space into the cyto- 1998a), such as by vacuolar sequestration in root cells (Zhang et al.,
plasm (Gaither and Eide, 2001) in plants and arthropods (see “uptake of 2020b). However, the mechanism(s) by which cations are loaded into
trace metals by arthropods” section). ZIP transporters have a broad sub- the xylem fluid are only partially understood (Kerkeb and Krämer,
strate range transporting Zn2+, Cd2+, Mn2+ and Fe2+ (Eide, 2006; Grotz 2003), as a process mediated by membrane transport proteins which
et al., 1998; Korshunova et al., 1999; Pence et al., 2000; Wu et al., 2009; can be energy-dependent (Kadukova and Kavulicova, 2011; Mori
Milner et al., 2013; De Oliveira et al., 2020). As for the detoxification of et al., 2009). For Cd and Zn, these metals are taken up mainly by ZIP
Zn within the plant, members of the MTP (metal tolerance protein) fam- transporters and loaded into the xylem by heavy metal ATPases
ily, from cation diffusion facilitator (CDF) family, are known to mediate Zn (Mendoza-Cózatl et al., 2011; Andresen et al., 2018). For instance,
transport from the cytoplasm into the vacuole (Gustin et al., 2009; HMA4 is considered a key transporter involved in Cd and Zn
Migocka et al., 2015). Yellow-stripe 1 like (YSL) proteins are believed to hyperaccumulation, as well as in xylem loading (Lochlainn et al.,
mediate the uptake of metals, particularly Fe, which are complexed 2011; De Oliveira and Tibbett, 2018), with its gene highly expressed in
with phytosiderophores or nicotianamine (NA) (Waters et al., 2006; the root pericycle of A. halleri (Hanikenne et al., 2008).
Socha and Guerinot, 2014). The most studied, YS1 from Maize, may also Transport of metal ions in the xylem vessels may be by simple bulk
play a role in metal homeostasis as it can also transport Zn2+, Cu2+ or transport or by a chromatographic exchange process: the exact process
Ni2+ (Haydon and Cobbett, 2007; Sinclair and Krämer, 2012), whilst appears to be dependent on the metal and the charge of the metal-
two other members of this transporter family – AtYSL4 and AtYSL6 – are ligand complex (Petit and van de Geijn, 1978). In both processes, trace
also involved in Ni2+ and Mn2+ homeostasis (Conte et al., 2013). Cd2+ metal translocation in the xylem is by mass flow in the transpiration
is also transported by the Nramp (= Natural resistance associated macro- stream (Luo et al., 2016). As a result, the quantity of trace metals
phage proteins) transporter, AtNramp, which is a Fe2+ transporter and translocated is proportional to the rate of transpiration (Grifferty and
LCT1, also transports Ca2+ (Clemens et al., 1998; Thomine et al., 2000; Barrington, 2000). Since the flux of some cations is related to water
Clemens, 2006; Migeon et al., 2010; Jha and Bohra, 2016). Nevertheless, flow, aquaporines and divalent-channel cations may mediate this pro-
as Cd is nonessential it is likely that it enters plant cells coincidentally, cess (Cabañero and Carvajal, 2007). The formation of chelate complexes
through transporters with low substrate-specificity; it is generally under- may determine the transport of metals in plants, for example, NA is in-
stood that Cd2+ uptake by plants happens by a carrier for Zn2+, or even volved in Cu and Ni transport in the xylem (Kadukova and Kavulicova,
other divalent cations, such as Cu2+ or Fe2+, or by Ca2+ and Mg2+ trans- 2011; Printz et al., 2016; Andresen et al., 2018). Citric and malic acids
porters/channels (Guerra et al., 2011; Clemens, 2006; Pottier et al., 2015). have also been linked to Cu transport in the xylem (Cao et al., 2020),
Analogous Nramp transporters have also been reported in arthropods however Cd was found to be in free ionic form in the xylem sap of
(see section on uptake by arthropods). With the established importance A. halleri (Ueno et al., 2008). In addition to vertical translocation from
of Cu2+ in processes such as electron transport, the COPT family of trans- root to shoot, there is also lateral translocation of trace metals through
porters involved in plant uptake of Cu were identified some time ago pits in the vessel walls. This results in the lateral translocation of ap-
(Kampfenkel et al., 1995; Sancenon et al., 2004; Burkhead et al., 2009), proximately 12% h−1 of the Cd2+ concentration within the xylem fluid
with several other members identified recently (Andresen et al., 2018). (Petit and van de Geijn, 1978).
The high affinity copper transporter, Arabidopsis COPT1, has a physiolog- Translocation of trace metals within plants also takes place via
ical role in root elongation and pollen development with the reporter phloem transport cells. Trace metals can enter the phloem sap by
gene highly expressed in embryos, trichomes, stomata, pollen and root selective transport from the xylem vessels within the stem or by
tips (Sancenon et al., 2004). Unlike Zn or Fe, Cu is taken up mainly as remobilisation from other plant tissues, especially at the nodes (Van
Cu+ by COPT1, but plants may also take up Cu2+ by members of the ZIP Bel, 1990) and leaf vein network (Pate et al., 1975). In wheat plants
family (Palmer and Guerinot, 2009). Proteins from the COPT family, the flag leaf and peduncle appear to be important sites for the transfer
which occur in a range of organisms, may be expressed during copper de- of trace metals between xylem and phloem (Herren and Feller, 1994,
ficiency, exhibit tissue-specific patterns and be influenced by endogenous 1997; Zeller and Feller, 1999). Two distinct processes are involved in
concentrations of Fe, Mn or Zn (Peñarrubia et al., 2010; Yuan et al., 2011). this transfer, the removal of metal from the xylem, and the loading of
For instance, a crosstalk between vacuolar Cu and Fe pools mobilisation in metal in phloem (Page and Feller, 2015). Transporters mediate uptake
A. thaliana was shown to involve the Cu-transporter COPT5, Nramp3 and into the symplast, and distribution within the leaf may occur via the
Nramp4. Whilst COPT proteins were more expressed in A. thaliana ex- apoplast or the symplast pathways (Kadukova and Kavulicova, 2011).
posed to Cd, suggesting that Cu uptake is an essential component for Cd Control mechanisms for these processes are separate, for instance, at
resistance in this species (Gayomba et al., 2013). high concentrations Zn2+ is eliminated from the xylem in the stem of
As cation transporters generally appear to have broad substrate wheat, where it is retained and not loaded into the phloem (Herren
specificity, competition for uptake between ions of the same charge is and Feller, 1994). Factors affecting the loading and unloading of trace el-
highly likely. This is assuming that the number of binding sites is ements in phloem are thought to be pH, Eh, ionic strength and organic
9
constituents within the phloem sap (Welch, 1995). For Cu, Fe and Zn, sap in the peduncle of wheat plants (Herren and Feller, 1994). Zn2+
NA is likely to be important for the phloem loading and unloading reaches the developing ear by being loaded into the phloem in this
(Curie et al., 2009). As in xylem fluid, trace metals in phloem sap are site (Herren and Feller, 1994). Wheat can control the loading of Zn2+
generally in the form of complexes rather than ions (Welch, 1995). into the phloem and thereby effectively regulate the Zn2+ concentration
Analyses in several plant species have shown that NA, glutathione and in the grain. In contrast, the extent of Cd2+ unloading in the peduncle is
phytochelatins (PCs) are the main metal-ligand molecules found in much less than Zn2+, and therefore translocation to the ears of wheat
the phloem sap, with NA forming complexes with Cu, Fe and Zn, and occurs by both xylem and phloem pathways (Herren and Feller,
glutathione and PCs with Cd, Zn and Hg (Mendoza-Cózatl et al., 2011; 1997). Nonetheless, recent studies in rice showed that Cd deposition
Komal et al., 2015). in grains was mediated by phloem transport, attributed to a transporter
Movement of trace elements within phloem is by mass transport, gene OsLCT1 identified to be highly expressed during reproductive
driven by the loading of phloem within source tissues and the unloading stages (Uraguchi and Fujiwara, 2012), whilst in wheat Cd was effec-
of sucrose at sink tissues (Welch, 1995), and can be greatly influenced tively remobilized from roots and stems, and accumulated in grains
by metal-ligands in the plant (Mendoza-Cózatl et al., 2011). The mobil- (Yan et al., 2019).
ity of metals within phloem varies with the metal and is also influenced Several protein families are involved in the long-distance transport
by competition between metals and, at high concentrations, the toxic of trace metals in plants, with the majority identified in A. thaliana.
effects of metals on phloem transport (Herren and Feller, 1997; Zeller The monovalent (Cu(I)) and divalent (Zn(II)/Cd(II)) cation transporting
and Feller, 1999). In young wheat leaves, phloem mobility of Ni and PIB-type ATPases are crucial in Cu and Zn translocation from root-to-
Zn was higher than the mobility of Co, Cd and Mn (Riesen and Feller, shoot, respectively (Hussain et al., 2004), whilst the ATPases HMA2
2005). Different ecotypes also have different phloem distribution pat- and HMA4 are a major mechanism for Cd translocation (Wong and
terns for the same metal, for instance hyperaccumulator Sedum alfredii Cobbett, 2009; Lochlainn et al., 2011). Proteins of the IREG family are
is able to relocate 44% of Cd to other organs via phloem, whilst its potentially involved in root-to-shoot transport of Ni and other transi-
non-hyperaccumulator ecotype only relocates 10% (Hu et al., 2019). tion metals (Kramer et al., 2007), as well as the NiCoT protein family
Phloem transport cells are metabolically active and may regulate the (Czajka et al., 2019). Finally, it has been hypothesised that YSL trans-
concentrations of trace metals and the form in which they are present porters, which transport metal complexes with NA and other LMW
in phloem sap (Welch, 1995). Phloem translocation can result in the re- compounds, may also be involved in long-distance transport of transi-
distribution of Cd2+, Co2+, Ni2+ and Zn2+ from the stem, flag leaf and tion metals and remobilisation from senescent tissues to reproductive
peduncle to the ears of winter wheat (Herren and Feller, 1997; Zeller organs (Haydon and Cobbett, 2007; Kramer et al., 2007; Sinclair and
and Feller, 1999; Riesen and Feller, 2005; Page and Feller, 2015) and a Krämer, 2012; Printz et al., 2016).
similar redistribution of Cd2+ may also occur in durum wheat
(Cieslinski et al., 1996). This redistribution of trace metal ions to the de- 3.4. Transformation of trace metals in plants
veloping grain may have an important influence on the exposure of sap
feeding insects to trace metals. Trace metals taken up by plants are transformed within the plant for
a number of reasons: to fulfil a range of metabolic plant functions; to de-
3.3.1. Metal distribution and sinks within the plant toxify excess concentrations of trace metals and render them metaboli-
Overall, the translocation of trace metals typically results in a pattern cally inactive; and to transport the complex mix of ions found in xylem
of distribution within plants where metal concentration falls in the fluid, some of which can be reactive or easily immobilised by hydrolysis
order root-shoot-reproductive organs (Lubben and Sauerbeck, 1991; (Clemens, 2006). The complexing ligands are predominantly organic
Cieslinski et al., 1996; Merrington et al., 1997a; Kabata-Pendias, 2010; acids and anionic and cationic amino acids/peptides (Cataldo et al.,
Gallego et al., 2012). Arthropod herbivory can affect this, with increased 1988; Cobbett and Goldsborough, 2002; Andresen et al., 2018; Chen
concentrations of Cd and Zn in the ears of wheat plants observed under et al., 2018). The type of ligand bound to a metal ion is metal specific
aphid infestation (Green et al., 2005), possibly as a defence mechanism and each metal may be bound to more than one type of ligand. How-
against herbivory (Gall et al., 2015). The binding of metal ions through ever, unbound, as well as bound, divalent metal ions also appear to be
storage/detoxification mechanisms within the root and mycorrhizal present within xylem fluid (Petit and van de Geijn, 1978; Cataldo
fungi are probably responsible for the high concentrations of metals et al., 1988; Mendoza-Cózatl et al., 2011; Lu et al., 2013).
within this organ (Hart et al., 1998b; Bellion et al., 2006; Saraswat and Zinc and nickel ions are complexed within the plant by organic acids
Rai, 2011; Gonzalez-Guerrero et al., 2016). However, there are large dif- and amino acids, but the actual ligands involved vary between plant spe-
ferences in the extent of root to shoot trace metal translocation among cies and plant tissues (Sinclair and Krämer, 2012). In grains and seeds,
plant species (Jarvis et al., 1976). Cadmium is an exception to the nor- Zn2+ is localized in globoid crystals, protein bodies mainly consisting
mal pattern as it is found in higher concentrations in leaves and bark of phytate, which form a stable complex with Zn2+ (Welch, 1995).
of some species such as poplars, flax and leafy vegetables such as spin- These complexes have also been identified in the roots, but not shoots,
ach (Cieslinski et al., 1996; Marzilli et al., 2018), as well as plants consid- of a range of crop plants and have been implicated in restricting root-
ered to be hyperaccumulators (Kramer, 2010; Gallego et al., 2012). shoot transport of Zn (Vansteveninck et al., 1994). High citrate and ma-
Translocation to the reproductive organs occurs directly via the late concentrations in Zn tolerant plants have also been correlated with
xylem pathway and also through redistribution via the phloem high internal Zn concentrations and Zn tolerance (Godbold et al., 1984;
(Herren and Feller, 1994; Cieslinski et al., 1996; Herren and Feller, Harrington et al., 1996). Other compounds that are proposed to bind Zn
1997; Zeller and Feller, 1998; Zeller and Feller, 1999; Mendoza-Cózatl in plants are organic acids, oxalate, phosphate, phytate and pectates
et al., 2011; Printz et al., 2016). The xylem pathway translocates trace (Sinclair and Krämer, 2012). Furthermore, in the hyperaccumulator
metals mainly to the vegetative parts of the reproductive organs, whilst Thlaspi caerulescens the majority of Zn2+ in the roots is complexed
the phloem pathway appears to be more important in translocation to with histidine, but is transported to the shoot in the xylem as a hydrated
the developing seed (Herren and Feller, 1994; Herren and Feller, cation, with a small proportion present as a Zn citrate complex. Once in
1997; Zeller and Feller, 1999; Mendoza-Cózatl et al., 2011; Deng et al., the shoot, Zn is mainly complexed with citrate with small concentra-
2018). The relative importance of xylem and phloem pathways in trans- tions bound to histidine, oxalate and the cell wall (Salt et al., 1999).
location depends on (i) the extent of unloading of the metal from the These complexes may be stored in the vacuoles of epidermal cells, and
xylem in the shoot, (ii) the relative mobility of the metal in the phloem the cell walls of epidermal and mesophyll cells (Kupper et al., 1999;
and (iii) the control the plant can exert on the loading of the metal in the Frey et al., 2000). Generally, trichomes and epidermal cells accumulate
phloem. For instance, the majority of Zn2+ is unloaded from the xylem the highest Zn concentrations, yet cell vacuoles probably make the
10
greatest contribution in storing excess Zn in leaves (Sinclair and Krämer, despite activating PC synthesis in algae (Mellado et al., 2012). In fact,
2012). PCs would be more pivotal in tolerance of non-essential metals, such
Nickel is mobile in the xylem and the phloem and is transported to as Cd and Hg, than in tolerance of toxic concentrations of essential
the shoots in both hyperaccumulators and non-hyperaccumulators metals (Hodson, 2012).
(Kochian, 1991; Riesen and Feller, 2005). In non-hyperaccumulators, With respect to MTs, whilst MT-like gene sequences have been iden-
Ni2+ is retained mainly in the roots, with a small proportion transported tified in plant tissues (Clemens, 2001), their function in plants is still un-
to the shoots. In hyperaccumulators Ni2+ is accumulated in the shoots: clear. There is some evidence they are involved in Cu tolerance and
however, the mechanism by which this occurs differs between plant homeostasis, and are up-regulated under metal excess (Cobbett and
genus. In Alyssum spp. xylem and shoot Ni2+ concentrations are Goldsborough, 2002). As yet there is still little molecular evidence of
strongly correlated with the histidine concentration, with histidine in- metal complexation by MTs within the plant (Clemens, 2006). How-
volved in both Ni2+ transport into the xylem and storage in the leaf ever, several studies have shown that the heterologous expression of
(Kramer, 2010). In the hyperaccumulator Thlaspi goesingense increased plant MT genes in yeast systems can increase tolerance and accumula-
vacuolar storage and the resultant Ni2+ tolerance is responsible for the tion of metals such as Zn, Cd and Cu (Kohler et al., 2004; Guo et al.,
hyperaccumulator phenotype, not high rates of root-shoot transport 2008; Yadav, 2010; Sheoran et al., 2011; Bulgarelli et al., 2016; De
(Kramer et al., 2000). However, histidine can sometimes suppress Ni Oliveira et al., 2020). In addition, MTs are involved in scavenging ROS
transport into root vacuoles and might even enhance root-to-shoot Ni (reactive oxygen species) in plant cells under stress through their Cys
flux (Kramer, 2010). Nickel in the shoots of both hyperaccumulators residues (Wong et al., 2004; Hassinen et al., 2011; Ruttkay-Nedecky
and non-hyperaccumulators is located in the apoplast, cytoplasm and et al., 2013).
vacuole, with hyperaccumulators storing Ni2+ in the vacuoles of epider-
mal cells (Psaras et al., 2000; Van der Ent et al., 2020). Additionally, in 3.5. Plants and multi-trophic metal transfer
hyperaccumulators from the Noccaea (Thlaspi) genus, a glutathione
concentrations can be positively correlated with the capacity of plants Plants play a major role in regulating the transfer of metals from soil
to accumulate and tolerate high Ni concentrations (Freeman et al., to arthropod, and should not be regarded as a neutral or passive carrier.
2004). In Festuca arundinacea, up-regulation of MT genes was also asso- Plants possess a variety of mechanisms for metal homeostasis and de-
ciated with Ni accumulation (Shabani et al., 2016). There are also varia- toxification which result in metals being partitioned and complexed
tions in the ligands binding Ni2+ in different plant species, with citrate, throughout the plant to varying degrees (see Sections 3.3 and 3.4).
malate, malonate, glutamine and histidine all identified as complexing Essential metals such as Cu, Zn and Ni are sequestered mainly in the
Ni2+ in plant shoots (Kramer et al., 1996). roots, with some restricted transport to shoots and reproductive organs.
The two most studied metal binding ligands in plant cells are PCs Cadmium, as a non-essential metal, has a higher propensity to accumu-
and MTs (Cobbett and Goldsborough, 2002; Andresen et al., 2018). late in tissues other than the roots, with the exception of known
PCs are a class of non-protein structures with increasing repetitions of excluder species, increasing the potential exposure of herbivorous ar-
Gly-Cys terminated by Gly, they are enzymatically synthesised – by glu- thropods, although this can vary between species and varieties. The
tathione and phytochelatin synthase – and generally induced by metal complexation, transport, partitioning and sequestration of metals in
and metalloid exposure (Rauser, 1990; Clemens, 2001; Garg and Kaur, planta can all affect the availability of metals and hence their subsequent
2013; Kaur and Garg, 2018). In contrast, MTs are small gene encoded transfer to herbivorous arthropods. These processes vary between plant
cys-rich proteins which complex metals, particularly Cu, in animals, species and also vary dependent on the internal metal load of the plant.
fungi and plants (Rauser, 1990; Hassinen et al., 2011). There is also a potential feedback mechanism in-play as arthropod her-
PCs are important for the transport and detoxification of Cd2+ and to bivory can affect the distribution of metals in plants (Green et al., 2005).
a lesser extent Cu2+ and Zn2+. In the cytosol PCs chelate Cd2+ to form
low molecular weight complexes which are translocated across the to- 4. Invertebrate herbivores
noplast via MTP and CDF proteins and sequestered in the vacuole of
cells (Clemens, 2006; Garg and Kaur, 2013; Lin et al., 2016). Once in Invertebrate herbivory affects all terrestrial plant families, although
the vacuole these complexes combine with more Cd2+, sulphur and the extent of herbivory will vary with the effectiveness of the plants de-
other PC chains to form high molecular weight complexes (Salt and fence mechanism (Kant et al., 2015), and can occur at a variety of stages
Rauser, 1995; Cobbett and Goldsborough, 2002; Kaur and Garg, 2018). in a plant's development and by a wide range of arthropod grazers. In-
There is also evidence from A. thaliana that PCs undergo long-distance deed, the phylum Arthropoda consists of a diverse range of organisms,
root-to-shoot and shoot-to-root transport, with root-to-shoot transport which is reflected in the diversity of trace metal concentrations found
resulting in reduced Cd2+ accumulation in roots (Gong et al., 2003; in the species of this phylum (Dar et al., 2019). This is the case among
Chen et al., 2006). even closely related species feeding on similar diets and is derived
The mechanism of Cu2+ and Zn2+ complexation is less clear with from inter-specific differences in physiology (Glowacka et al., 1997;
conflicting evidence on the complexes involved. Cu2+ has a high affinity Janssen et al., 1991; Laskowski and Maryanski, 1993; Rabitsch, 1995;
for peptide and sulfhydryl groups e.g. cysteine-rich proteins, as well as Sá et al., 2008), which results in some species exhibiting a poor ability
carboxylic and phenolic groups. Consequently, in roots and xylem sap to regulate internal trace metal concentrations (Dallinger, 1993;
>98% of Cu2+ is complexed (Marschner, 2012). PCs (cys-rich proteins) Janssen et al., 1991; Kramarz, 1999b). This section examines the physi-
are involved in the homeostasis of Cu2+ and Zn2+ (Tennstedt et al., ology of arthropods that affects the transfer and accumulation of trace
2009). Their induction by Cu2+ and the formation of Cu-PC complexes metals from their food.
has been proven using HPLC-ICP-AES in Rubia tinctorum root cultures
(Maitani et al., 1996). There is no information available on the localiza- 4.1. Availability of trace metals to herbivorous arthropods
tion or storage of Cu-PC complexes; however, we postulate that they are
located and transported in the same way as Cd-PC complexes, described The most obvious factor governing the input of metals to herbivo-
above. In a study with several plant species growing in a contaminated rous arthropods is the concentration and form of the trace metal in
mining area, Machado-Estrada et al. (2013) verified greater accumula- the plant tissues and cells consumed (section 2) which can affect the ab-
tion of Cu in stems of Euphorbia prostrata, whilst low accumulation of sorption of the metal by arthropods (Hare, 1992). For example, metals
thiol-containing molecules, suggesting that PCs were not much in- in an insoluble form, such as bound to cell wall components, may be
volved in Cu accumulation. Unlike Cd, PCs would not be a primary factor digested and absorbed with difficulty, whilst metals in an ionic form
in determining Cu tolerance (Lee and Kang, 2005; Hego et al., 2014) and in dissolved complexes, such as in the vascular fluids, may be
11
readily absorbed (Cataldo et al., 1987; Dar et al., 2017; Dar et al., 2019), utilised by plant cells, but metal uptake in arthropods has received con-
although ingesting whole plant material appears to increase overall bio- siderably less attention than in plants. Nevertheless, trace metal uptake
accumulation (Butt et al., 2018). The transfer of metallic nanoparticles by arthropod cells is complex with the uptake of a given metal poten-
from plant to insects can also occur, as demonstrated by Kubo-Irie et al. tially proceeding through more than one uptake system (Fig. 4) and in-
(2016), in which TiO2 nanoparticles were effectively taken up by the dividual transport systems often exhibiting poor discrimination among
host plant (Aristolochia debilis), translocated to the leaves and eventually elements, transporting several metals with similar physio-chemical
transferred to the larvae of the swallowtail butterfly (Atrophaneura properties. This later point is particularly important in the uptake of
alcinous). non-essential trace metals for which specific uptake mechanisms have
not evolved.
4.2. Uptake of trace metals by arthropods The primary uptake mechanism for the essential elements Cu and Zn
have been clearly established. For Cu, the Cu+ transporter Copper
By far the greatest input of trace metals into the soma of arthropods Transporter 1B (Ctr1B) is the most efficient importer of Cu into the
is through the ingestion of food (Janssen et al., 1993). Absorption of enterocytes of larval Drosophila melanogaster (Balamurugan et al.,
trace metals through the integument of terrestrial arthropods is thought 2007). Expression of Ctr1B is much lower in adult D. melanogaster and
to account for only a minor proportion of metal uptake (Janssen et al., the expression of the related Cu transporter Ctrl1A suggests that this
1993; Vijver et al., 2005). Hence, the alimentary canal is the primary protein may be more important in Cu acquisition in adult flies (Zhou
site of trace metal absorption. In arthropods, this organ consists of et al., 2003). Consequently, differing, although related, mechanisms
three regions, the foregut, midgut and hindgut. Both the foregut and can be active in the developmental stages compared to the adult
hindgut are lined with cuticle, which leaves the midgut as the major stage, reflecting the nutrient demands of growth and development.
site of nutrient and trace metal absorption (Chapman, 1998). Mammalian divalent metal transporter 1 (DMT 1, also designated
Trace metals are absorbed as free ions, which precludes uptake by Nramp2, SLC11A2, and DCT1) actively transports a number of divalent
simple diffusion over the plasma membrane. Uptake therefore proceeds cations, including Fe2+, Cu2+, Cd2+ and Ni2+ (Bressler et al., 2004;
via active transport proteins and facilitated diffusion through ion chan- Gunshin et al., 1997; Illing et al., 2007), but not Zn2+ or Pb2+, into
nels. The active transporters involved are closely analogous to those cells (Bannon et al., 2003; Sacher et al., 2001). Malvolio (Mvl), the insect
Fig. 4. Metal trafficking pathways in arthropod cells. MT – bound to metallothioneins, Glut – bound to glutathionone, A – incorporated into type A metal rich granule, B – incorporated into
type B metal rich granule, ApoPro – transferred to apometalloproteins, MetChap – bound to metallochaperones, Pep – bound to low molecular weight polypeptides/proteins, organelle –
sequestration within organelles other than lysosomes, SP – export via the secretory pathway, dashed lines – possible pathway. Uptake proteins in bold are the primary proteins involved in
metal uptake.
12
orthologue of DMT 1 (Folwell et al., 2006; Martínez-Barnetche et al., extra- to inter-cellular proton gradient for transport (Bannon et al.,
2007), is a functional Fe and Cu transporter (Martínez-Barnetche et al., 2003; Elisma and Jumarie, 2001; Gunshin et al., 1997; Okubo et al.,
2007; Southon et al., 2008). Indeed, despite the demonstrated impor- 2003); transport by DMT 1 appears to be negligible at pH < 7 (Elisma
tance of Ctr transporters for Cu acquisition, functional Mvl also appears and Jumarie, 2001; Okubo et al., 2003). Typical midgut pH values for ar-
to be necessary for optimal Cu acquisition (Southon et al., 2008) thropods tend towards pH 6.0–6.5, which should be sufficient for DMT
As described for plants, Zn2+ influx transporter proteins of the Zrt/ 1/Mlv transport (Okubo et al., 2003; Martínez-Barnetche et al., 2007).
IRT-like protein (ZIP) family function as the main mechanism for Zn up- Members of the ZIP family, which in the case of mammals have also
take in Arthropods (Navarro and Schneuwly, 2017). The number of pu- been reported to transport Ni2+ (Dempski, 2012), are a second potential
tative ZIP proteins sequences in the genome of D. melanogaster ranges pathway for Ni uptake.
between 8 and 10 (Gaither and Eide, 2001; Taylor and Nicholson,
2003; Wang et al., 2009) and ZIP sequences are also reported from 4.3. Transformations of trace metals in arthropods
other Arthopods (Taylor and Nicholson, 2003). The importance of the
ZIP transports for Zn uptake by D. melanogaster has been clearly Once absorbed by cells, trace metals can be exported from the cell or
established (Lye et al., 2012). be transformed in both the cytosol and within organelles. Transforma-
Cadmium has no known biological function in Arthropods and whilst tions may be for the beneficial use of the organism or if the trace
Ni has a limited biological role in eukaryotes, Arthropods lack the genes metal is in excess, to render the metal metabolically inactive to avoid
for the enzyme utilizing Ni as a cofactor and the gene coding for the eu- toxicity (Fig. 4). The diversity of the Arthropod phylum is reflected in
karyotic Ni transporter (Zhang et al., 2009). Thus, in contrast to Cu and the sites and nature of trace metal transformations (Sá et al., 2008).
Zn, no specific uptake mechanisms exist for Cd or Ni in Arthropods However, some generalities can be made. Beneficial transformations
and uptake must proceed through mechanisms evolved for the acquisi- are principally the inclusion of trace metals into the active sites of
tion of essential elements. enzymes, metallochaperones, respiratory pigments, transcription fac-
The potential mechanisms for Cd uptake are principally the active tors and into the exoskeleton (Chapman, 1998; Quicke et al., 1998;
transporters DMT 1 and ZIPs and Ca2+ channels. Investigations of Cd up- Schofield et al., 2002; Vijver et al., 2004). Transformations to avoid tox-
take via DMT 1 in whole mammals, mammal cells or using mammalian icity are principally biomineralisation via inclusion into mineral rich
DMT 1 expressed in Xenopus oocytes, suggest that DMT 1 can play a sig- granules (MRGs, also called mineral spherites) or binding to specific
nificant role in Cd2+ uptake (Bressler et al., 2004; Okubo et al., 2003; metal sequestering proteins/peptides (Hopkin, 1989; Dallinger, 1993;
Park et al., 2002; Ryu et al., 2004). Similarly, ZIP transporters from Vijver et al., 2004; Pedersen et al., 2008).
yeast, plants and mammals are able to to transport Cd2+, but they Trace metals appear to be initially rendered metabolically inactive
have a lower affinity for Cd2+ than Zn2+ (Gitan et al., 1998; Clemens, through binding to short chain peptides or proteins, predominantly gluta-
2006; Cohen et al., 2004; Dalton et al., 2005; Fujishiro et al., 2009; thione and MTs (Martoja et al., 1983; Marioni and Watson, 1985; Singhal
Girijashanker et al., 2008; Gitan et al., 1998). On this evidence and the et al., 1987; Hopkin, 1989). The iron sequestering protein ferritin may also
conserved nature of transporters in eukaryotic cells, it is highly likely function in this role as it can bind Cd, Cu and Zn (Joshi and Zimmerman,
that Mvl and ZIPs transport Cd2+ into Arthropod cells, but this remains 1988) and the genes coding for ferritin light and heavy chains in
to be tested experimentally. D. melanogaster are induced by Cd, Cu and Zn (Yepiskoposyan et al.,
Research has also strongly implicated calcium channels in Cd uptake 2006). In contrast, genes coding for metallochaperones show no increase
by invertebrates at the cellular (Braeckman et al., 1999) and organism in transcription in response to elevated metal exposure, suggesting that
level (Craig et al., 1999). However, He et al. (2009) suggested that they do not function in trace metal detoxification (Southon et al., 2004).
based on reported affinities, transport by ZIP proteins could be more im- Glutathione and MTs are pivotal in the homeostasis and detoxifica-
portant to the transport of Cd into cells than either calcium channels or tion of trace metals in Arthropod cells under acute exposure. Glutathi-
DMT 1 at environmentally relevant concentrations. Indeed, in MT-1 and one is a tripeptide (γ-Glu-Cys-Gly), which, among a variety of roles,
-II knockout cells, ZIP 8 knockdown reduced Cd accumulation by 35%, can bind metal(loid)s, including Cd, Cu, Ni, and Zn (Ballatori, 1994;
but DMT 1 knockdown had a minimal effect (Fujishiro et al., 2009). Kręźel and Wojciech, 2004; Burford et al., 2005). Glutathione is present
Moreover, Cd resistance in two cell lines derived from the MT knockout in relatively high (millimolar) concentrations within cells, which means
cells was not related to changes in T-type Ca2+ channel expression that there is sufficient glutathione to rapidly bind and effectively detox-
(Fujishiro et al., 2009). ify metallic cations as they enter the cell (Singhal et al., 1987; Freedman
The studies discussed above strongly suggest that Cd can be taken up et al., 1989; Ballatori, 1994; Conners and Ringwood, 2000; Zaroogian
via multiple pathways. However, there is a tissue/cell specific expres- and Norwood, 2002). This is essential as there is a lag of several hours
sion of each type of transporter (Fujishiro et al., 2009; Girijashanker between increased metal concentrations and the rise in MT or MT-like
et al., 2008; Martínez-Barnetche et al., 2007; Wang et al., 2009), which protein (MTLP) levels in the cell (Everard and Swain, 1983; Ochi et al.,
results in various uptake pathways in different cells, complicating at- 1988; Freedman et al., 1989). Binding of the metallic ions by glutathione
tempts to elucidate critical Cd uptake pathways. Moreover, the relative appears to effectively protect cells from Cd (Singhal et al., 1987; Ochi
contribution of these ones will almost certainly vary depending on the et al., 1988) and Cu (Freedman et al., 1989) toxicity during this lag.
presence of competition from the transporters' intended substrate, the Moreover, in both mammals and invertebrates, the formation of the
concentration of the intended substrate (which will affect expression MT-Cu complex appears to require glutatione, possibly because the for-
of the transporter) and, in the case of secondary active transporters re- mation of the complex requires glutatione to transport Cu to the MT
quiring H+, the pH of the gut lumen (Gitan et al., 1998; Illing et al., 2007; molecule (Freedman et al., 1989; Ferruza et al., 2000; Zaroogian and
Ryu et al., 2004; Wang et al., 2004). Norwood, 2002).
Rapid accumulation of Ni is exhibited by some arthropods The role of MTs in metal detoxification has been the subject of some
(Bednarska and Laskowski, 2008; Boyd, 2009; Bednarska et al., 2011; debate, but D. melanogaster null mutants for all MT genes showed in-
Green and Walmsley, 2013), which most likely occurs via iron and creased sensitivity to Cd and Cu stress (Egli et al., 2006; Yepiskoposyan
zinc transporters (Klein and Costa, 2015). DMT 1 actively transports et al., 2006), strongly suggesting that MTs provide a mechanism for
Ni (Illing et al., 2007) and has been implicated in Ni uptake in rat jejunal the detoxification of trace metals. However, this mechanism does not
segments (Muller-Fassbender et al., 2003). However, this raises an issue function effectively for all trace metals. This is particularly evident for
for some insects with a high midgut pH, such as the Lepidoptera and Zn in the Hexapoda, which in contrast to the situation in vertebrates,
those that feed on hemicellulases (Chapman, 1998; Gullan and show a poor ability to synthesise MTs in response to Zn exposure and
Cranston, 2005), as DMT 1 is a Me2+/H+ symporter that requires an the MTs produced by them have a poor ability to bind Zn (Marioni and
13
Watson, 1985; Maroni et al., 1986; Zhang et al., 2001a, b; Sterenborg associated with MTLPs (Martoja et al., 1983; Dallinger and Prosi, 1988;
et al., 2003; Egli et al., 2006a, b; Capdevila et al., 2010). Furthermore, Barka et al., 2001; Nunez-Nogueira et al., 2006). A relatively small pro-
MT null mutants of D. melanogaster show no increased sensitivity to portion of Zn is found in MRGs, perhaps due to the instability of the
Zn stress (Egli et al., 2006a, b; Yepiskoposyan et al., 2006). Little data Zn-thiolate complex in the low pH of lysosomes. Consequently, Zn
are available for the other Athropod subphyla, but crustacean MT can could be liberated from MT before MRG formation with the result that
bind both Zn and Cu (Valls et al., 2001; Capdevila et al., 2010), which Zn is exported back into cytosol (Amiard et al., 2006). The binding of
suggests MTs may play a more prominent role in Zn homeostasis in at Ni to MT is even less stable than for Zn (Nielson et al., 1985) and conse-
least this subphyllum. Overall, it has been suggested that MTs are quently only a small proportion of Ni is found in MRGs (Geffard et al.,
more important for non-essential elements such as Cd, which lacks spe- 2010).
cific efflux pathways and needs to be detoxified by remaining tightly
bound in the cytosol (Ardestani et al., 2014). 4.3.1. Sites of trace metal sequestration
The relatively weak induction of and binding to MT/MTLPs by Ni sug- The taxonomic diversity of the Arthropoda is reflected in the diver-
gests that MTs also do not play an important role in the regulation of Ni sity of the organs responsible for trace metal regulation and/or stor-
(Nielson et al., 1985; Barka et al., 2001; Amiard et al., 2006). Barka age/detoxification. However, in all groups the efficiency of the MT/
(2007) suggested that metalloproteins other than MTs bind Ni in the cy- MRGs to sequester trace metals can efficiently prevent the majority of
tosol. However, the determination of Ni-MTLP levels is sensitive to the trace metals passing through the gut epithelia for distribution to the
method used and that Ni binding to MTLPs may be underestimated wider soma of the organism. As a result, the mid-gut and associated
(Geffard et al., 2010) structures are the primary site of metal accumulation. In the sub-
Typically 3–5 isoforms of MTs are reported for Arthropod species phyla Chelicerata and Crustacea, extensive accumulation of Cd, Cu and
(Syring et al., 2000; Ahearn et al., 2004; Egli et al., 2006a, b), although Zn occurs in well-developed mid-gut diverticulae, which form a struc-
information is again lacking for many taxa. Isoforms differ in their ability ture called the hepatopancreas (Hopkin, 1989; 1990; Morgan et al.,
to bind Cd and Cu such that one isoform will preferentially bind Cd and 1990; Köhler, 2002; Vijver et al., 2005). Very high concentrations of
another Cu. Exposure to one of these metals results in the preferential trace metals can be accumulated in this organ. For example, the hepato-
induction of the gene for the MT isoform that preferentially binds that pancreas of the isopod Porcellio scaber can accumulate concentrations of
metal (Dallinger et al., 1997; Egli et al., 2006a, b; Yepiskoposyan et al., over 1250 mg kg−1 Cd, 19,000 mg kg−1 Cu and 21, 000 mg kg−1 Zn
2006). Consequently, MTs provide a flexible system, allowing cells to re- (Hopkin, 1990a, b).
spond to elevated concentration of one trace metal, whilst having a The sub-phyla Myriapoda and Hexapoda lack developed mid-
minimal effect on the homeostasis of essential metals. diverticula and the mid-gut itself is the principle site of Cd and Cu,
Whilst glutathione/MTs function in the initial scavenging of trace and to a lesser extent Ni and Zn, storage/detoxification (Sohal et al.,
metals, longer term storage appears to be the function of MRGs. Thus, 1977; Aoki and Suzuki, 1984; Marioni and Watson, 1985; Maroni
the ultimate fate of metal bound to MT would be incorporation of the et al., 1986; Crommentuijn et al., 1994; Rabitsch, 1997; Köhler, 2002;
metal into intracellular MRG via a process of biomineralisation. This oc- Migula et al., 2007; Bednarska et al., 2019). For example, 92% of the Cd
curs in the lysosomal system of the cell (Hopkin, 1989; Barka, 2007). in the body of the collembolan Orchesella cincta was found in the gut
However, the processes involved in the transport of MT into the lyso- (Hensbergen et al., 2000).
some and incorporation of metal into MGRs is not fully understood. The accumulation of Cd, Cu, Ni and Zn in the malpighian tubules (the
Moreover, excess Cu and Zn ions may also be ‘scavenged’ from the cyto- organ responsible for osmo-regulation, ionic balance and excretion of
plasm by importation directly into the lysosomes via transmembrane nitrogenous waste in the Hexapoda, Myriapoda and Chelicerata) sug-
transporters such as Nramp2 (Martínez-Barnetche et al., 2007; gests that they function in the removal and storage/excretion of excess
Sterling et al., 2007) and ZnT35C (Tejeda-Guzmán et al., 2018). Such a trace metals from the haemolymph (Martoja et al., 1983; Lindqvist
mechanism is analogous to vacuolar scavenging in plant cells. This et al., 1995; Rabitsch, 1997; Schofield et al., 1997; Bradley, 1998;
mechanism would allow the lysosomal/MRG system to potentially con- Przybylowicz et al., 2003; Migula et al., 2007; Leonard et al., 2009; Yin
tribute to the rapid removal of excessive trace metal ions from the cyto- et al., 2017). The importance of this organ in trace metal storage/regula-
sol prior to MT synthesis and could represent an important tolerance tion can be judged by the fact that the highest concentrations after the
mechanism, as it does in plants. mid-gut are found in the malpighian tubules (Rabitsch, 1997). Cd and
Metal-rich granules are reported to be produced by the Hexapoda Zn are stored in MRGs within the cells of malpighian tubules and this
(Pawert et al., 1996; Pigino et al., 2005), Myriapoda (Vandenbulcke site may be important in the long-term accumulation of these elements
et al., 1998a; Köhler et al., 1995), Chelicerata (Ludwig and Alberti, (Sohal et al., 1976; Zierold and Wessing, 1990; Smit and van Gestel,
1988; Pigino et al., 2006) and Crustacea (Hopkin and Martin, 1982; 1996; Tejeda-Guzmán et al., 2018). The form of Cu and Ni in the malpi-
Schill and Kohler, 2004). Metal-rich granules are produced in tissues ghian tubules is not currently understood, but storage in MRGs may be
where trace metals are accumulated (see below) and increase in number predominant.
and/or metal concentration in relation to the exposure of the organism to Arthropods possess anthrocyte cells, which also remove sub-
trace metals (Martoja et al., 1983; Pawert et al., 1996; Vandenbulcke stances from the haemolymph. Anthrocytes (also known as pericar-
et al., 1998a; Vandenbulcke et al., 1998b; Schill and Kohler, 2004; dial cells, garland cells or nephrocytes) are associated with the fat
Pigino et al., 2006). Metals incorporated in to MRGs are insoluble and body and pericardium in the Hexapoda, Myriapoda and Chelicerata
therefore unavailable to take part in, or disrupt, the metabolic activity and gills of the Crustacea. These cells actively take up haemolymph
of the cell (Hopkin, 1989). by pinocytosis and principally function in the regulation of proteins
Hopkin (1989) described four types of MRG, termed A–D. Only types in the haemolymph (Locke and Russell, 1998). However, large accu-
A and B sequester trace metals (Type C and D MRGs are described as se- mulations of Cd, Pb and Zn occur in MRGs within anthrocyte cells
questering Fe and Ca respectively). Type A granules are formed by con- (Martoja et al., 1983; Vandenbulcke et al., 1998b; Nunez-Nogueira
centric layers of calcium and magnesium phosphates in which Zn can be et al., 2006) and hence may have a significant role in removing
sequestered (Hopkin, 1989). Type B granules contain a high proportion trace metals from the haemolymph (Martoja et al., 1983). Conse-
of sulphur and chalcophilic elements such as Cd and Cu, but Zn may also quently, anthrocytes may be central to the regulation of trace metals
be incorporated (Hopkin, 1989). Ni is reported to be incorporated into in the haemolymph of arthropod groups such as the Aphidae and
MRGs containing Ca, Mg, P, S and Cu and Zn (Barka, 2007), which sug- Collembola that do not possess malpighian tubules.
gests that it is found in both type A and B MRGs. Cu is more readily in- Structural components of arthropods, such as the integument, can
corporated into the lysosomal/MRG system than Cd, which is more also be important sinks for trace metals. For example, Cd, Cu, Ni and
14
Zn have been reported in arthropod exoskeletons (Hopkin and Martin, increased sensitivity to Cd exposure (Yepiskoposyan et al., 2006), indi-
1983; Schmidt and Ibrahim, 1994; Amyot et al., 1996; Schofield et al., cating that at best, efflux by this protein plays a minor role in preventing
2002; Green et al., 2003; Przybylowicz et al., 2003; Pourang et al., Cd toxicity. Consequently, the pathways for Cd and Ni export remain
2004; Boyd et al., 2007; Migula et al., 2007). The proportion of the somewhat enigmatic.
total body burden of these metals found in the exoskeleton varies
with metal and species (Orlowski et al., 2020), but is typically in the 4.3.3. Transport of trace metals within arthropods
range of 10% to 30% (Hopkin and Martin, 1983; Andrzejewska et al., The major mechanism for transporting substances absorbed through
1990; Amyot et al., 1996; Green et al., 2003; Dar et al., 2015). Cu gener- the gut around the body of Arthropods is via the open circulatory sys-
ally appears to be deposited in the exoskeleton to the greatest extent, tem in the haemolymph (Donker et al., 1990; Donker et al., 1996;
followed by Zn > Cd > Ni (Amyot et al., 1996; Green et al., 2003). How- Martin and Rainbow, 1998). Trace metals enter haemolymph over the
ever, exceptions to this generalisation exist (Orlowski et al., 2020). For basolateral surface of the mid-gut through the action of the transporters
example, the centipede Lithobius variegatus had 45–60% of its Zn body discussed in the preceding section. In the haemolymph, trace metals are
burden in the exoskeleton, compared to 7–26% for Cu and 5–12% for predominately bound to proteins, with the free ion accounting account
Cd (Hopkin and Martin, 1983). Transformation of trace metals into for as little as 0.01% of the trace metal in haemolymph (Bryan, 1966;
structural components is most striking in chewing herbivorous insects, Donker et al., 1990; Martin and Rainbow, 1998).
the mandibles of which can contain up to 25% Zn (Schofield et al., 2002).
The ovipositors of some hymenpoterous insects can also contain high Zn 4.4. Regulation of trace metals by cells
concentrations, up to 10% by weight (Quicke et al., 1998). In both in-
stances, the role of Zn in the exoskeleton is to increase hardness Organisms and their constituent cells face a difficult balancing act to
(Quicke et al., 1998; Schofield et al., 2002). Moreover, in populations maintain a homeostatic supply of essential trace metals for the cell's
of the beetle Lucanus cervus, no correlation was found between abdo- metabolism, whilst preventing excess levels of essential and non-
men and exoskeleton concentrations of Zn and Cu – indicating poor traf- essential metals causing stress and damage. Consequently, the uptake,
ficking from gut to exoskeleton and more homeostatic control – whilst efflux and sequestration of trace metals can be regulated through a
concentrations of Cd and Ni had a positive correlation between these number of mechanisms. These include translation and post-translation
two compartments (Orlowski et al., 2020). control of the proteins involved.
To prevent the accumulation of a substance, individual cells can con-
4.3.2. Export of trace metals from cells trol the number of transport proteins localized to the plasma membrane
Metallic cations can leave cells through the Golgi secretory pathway and thereby control the flux of trace metals into the cell. ZIPs proteins
or via active transport over the plasma membrane. As with plants, involved with metal uptake are constantly trafficked between the
members of the Cation Diffusion Facilitator (CDF) family of proteins plasma membrane and endosomes, with Zn deficiency decreasing en-
and P1B-type ATPases are fundamental to trace metal efflux. docytosis to increase the level of transporter in the plasma membrane
For Zn, the most important transporters are the Zinc Transport (ZnT) (Bowers and Srai, 2018). Conversely, excess Zn rapidly changes the
proteins, which are CDF members (solute carrier 30A family — SLC30A). localisation of ZIPs from the plasma membrane to endosomes (Kim
For Cu, the P1B-type ATPase ATP7 seems to be the only efflux transporter et al., 2004; Wang et al., 2004; Hara et al., 2017), reducing the flux of
(Norgate et al., 2006). Both ZnT (ZnT35C and ZnT1) and ATP7 are Zn into the cell. Degradation of the ZIP protein by lysosomes may follow
expressed in Drosphila midgut cells (Southon et al., 2004; Norgate endocyctosis (Hara et al., 2017; Bowers and Srai, 2018), potentially re-
et al., 2006; Yepiskoposyan et al., 2006; Wang et al., 2009). They may ducing the pool of ZIPs available for trafficking back to the plasma mem-
be essential for the transfer of trace metals absorbed by the mid-gut ep- brane and thereby maintaining reduced metal flux.
ithelium into the wider soma and to prevent the build-up of toxic con- Copper dependent transcription level control, but not endocytosis,
centrations of trace metals (Southon et al., 2004; Norgate et al., 2006; has been demonstrated for Ctr1B in D. melanogaster (Balamurugan
Yepiskoposyan et al., 2006; Bahadorani et al., 2010; Binks et al., 2010; et al., 2007). Simarly, Turski and Thiele (2007) found Ctr1A was largely
Lye et al., 2012). localized to the plasma membrane, but they did not study the trafficking
Both Cu and Zn are also exported from cells by the secretory path- of the protein. Studies investigating the trafficking of mammalian Ctr1
way in golgi derived vesicles as part of the normal metabolism of demonstrated reversible trafficking of Ctr1 from the plasma membrane
metalloproteins (Eide, 2006; Lutsenko et al., 2007). Experimental evi- into endosomes following exposure of cells to Cu excess (Petris et al.,
dence also suggests that Cd can leave cells when transported into 2003; Clifford et al., 2016), with recycling of Ctr1 back to the cell surface
golgi vesicles by Ca2+-ATPases instead of Ca2+ (Lauer Júnior et al., occurring rapidly (~15 min) following removal of excess Cu (Clifford
2008). However, it is not clear if the secretary pathway has any role in et al., 2016). As with ZIPs, elevated Cu also resulted in the degradation
preventing Cd toxicity. of Ctr1 proteins in mammal cells (Petris et al., 2003).
No efflux transporters of Cd and Ni have been reported from arthro- The ZnT Zn efflux transporters can also be trafficked to the plasma
pods. In mammals, there is evidence that the Fe2+ efflux transporter membrane in response to excess Zn and from the cells' surface under
Ferroportin (FPN1, also designated Metal Transporter Protein 1, Zn deficiency to regulate Zn (Hara et al., 2017; Nishito and Kambe,
scl40a1, Ireg1) can also transport Cd2+ and Ni2+ (Ryu et al., 2004) 2019). Trafficking of the Cu efflux transporter ATP7 is less clear. The ma-
and A. thaliana Ireg2 is also a Ni efflux transporter (Schaaf et al., jority of ATP7 is reported to be localized to the plasma membrane
2006). Given the function of homologous transporters seems well con- (Norgate et al., 2006; Burke et al., 2008; Zhang et al., 2020a), with
served in eukaryotes, it is highly likely that this Fe pathway transports some intracellular localisation, probably to supply Cu to the trans-
Cd and Ni. However, whilst FPN1 is strongly conserved from plants to golgi network. However, there is little evidence of trafficking between
animals and is present in arachnids, insects lack the gene for this protein the two locations (Mercer et al., 2017). Consequently, transcription
(Tang and Zhou, 2013) and therefore it cannot explain Cd and Ni export level control of ATP7 is likely the main mechanism of Cu efflux
in this class. regulation.
Another possible mechanism for Ni and Cd export is via CDF trans- Key to the transcription level regulation of free metal ions in the cell
porters. Cd can induce ZnT35C (Yepiskoposyan et al., 2006), suggesting is the zinc finger transcription factor metal response element binding
that this Zn efflux transporter may transport Cd, whilst some members transcription factor 1 (or metal-responsive transcription factor 1;
of the ZnT family can transport both Cd and Ni (Montanini et al., 2007). MTF-1). The MTF-1 protein has a strongly conserved zinc finger domain
Direct Cd and Ni transport by arthropod ZnTs has not yet been shown that is able to sense free Zn2+ in the cell through a direct and reversible
and D. melanogaster with a truncated ZnT35C gene did not show interaction between the ion and zinc finger domain (Dalton et al., 1997).
15
In insects, a second cysteine-rich domain senses Cu+ through binding of 2012). Of these, dZnT35C is expressed on the apical surface of malpi-
the ion to this domain (Chen et al., 2018). MTF-1 can also sense Cd and ghian tubule cells of larval D. melanogaster (Yin et al., 2017) and is
Ni levels in the cell, possible via the release of Zn2+ into the cytoplasm thought to be fundamental to the removal of Zn from malpighian cells
following displacement of Zn from pools in the cell, particularly MTs, by into the tubule lumen and regulation of Zn concentrations in the body
these two metals (Zhang et al., 2003; Nemec et al., 2009). The interac- (Yepiskoposyan et al., 2006; Yin et al., 2017). Cadmium is also secreted
tions between Zn/Cu begin the activation MTF-1, which is translocated into the fluid in the tubule lumen at a rate that can significantly remove
into the nucleus, subsequently binding to metal response elements in Cd from the haemolymph (Leonard et al., 2009). MRGs have also been re-
the promoter regions of specific genes, altering the transcription of ported in the lumen of the malpighian tubules (Spring and Felgenhauer,
these genes. Increased transcription is seen for the genes coding for 1996), suggesting that trace metals in this form can be excreted by this
MTs (Yepiskoposyan et al., 2006) and ferritin (Yepiskoposyan et al., organ along with ionic forms.
2006; Günther et al., 2012), increasing the cell's ability to sequester The homologous structures of arachnids (malpighian tubules and
metals. Increased transcription also occurs for the genes for the efflux coxal glands) and crustaceans (atennal glands) potentially have a simi-
transporters ATP7, ZnT35C, ZnT63C (Yepiskoposyan et al., 2006; lar role. The antennal glands of crustaceans can certainly remove Cd
Günther et al., 2012) and FNP1 (Troadec et al., 2010), allowing the cell from the haemolymph (Rouleau et al., 2001), but a role in the excretion
to export excess trace metals. MTF-1 can decrease expression of the of trace metals from the body remains to be established.
ZIP10 and Ctr1B (Yepiskoposyan et al., 2006; Günther et al., 2012), po- Juvenile Arthropods and species which moult as adults can also lose
tentially reducing uptake of Zn and Cu. However, there is no evidence trace metals through sequestration into the exoskeleton, which is then
that MTF-1 affects the expression of Ctr1A (Yepiskoposyan et al., lost when shed during moulting or in the pupal exuviae (Andrzejewska
2006). Indeed, it seems for Cu that D. melanogaster is not able to respond et al., 1990; Lindqvist and Block, 1994; Hensbergen et al., 2000; Green
to potentially toxic Cu concentrations by decreasing uptake by the mid- et al., 2003; Przybylowicz et al., 2003; Raessler et al., 2005; Boyd,
gut and instead relies on the export of excess ions across the basolateral 2009; Dar et al., 2015). As with other aspects of trace metal physiology,
membrane into the haemolymph to prevent toxicity to the epithelial the extent to which an element is eliminated by this mechanism can dif-
cells (Norgate et al., 2006; Southon et al., 2004). fer markedly between even closely related species (Raessler et al.,
Taken together, these mechanisms outlined above demonstrate that 2005).
at the cellular level, Arthropods have the means to effectively deal with
exposure to excess (and indeed, deficient) levels of trace metals, espe- 4.6. Herbivorous arthropods and multi-trophic metal transfer
cially essential ones. However, for the organism, mechanisms that rely
on the export of excess metal from the cell pass the problem on to Herbivory is the crucial step responsible for introducing metal con-
other cells/tissues. Hence, the organism either has to excrete the excess taminants into the animal kingdom. The majority of trace metals taken
metal from the body or have sufficient capacity to store the metal in a de- up by the transport proteins of the mid-gut epithelium cells in arthro-
toxified state. The latter strategy is risky in that when the storage/detox- pods are held there or in structures associated with the mid-gut,
ification capacity of critical tissues/organs is exceeded, toxicity can quickly preventing toxicity by being either bound to polypeptides/proteins
follow on further uptake of metals (Hopkin, 1990a; Crommentuijn et al., such as MTs or included into MRGs formed by lysosomes. A relatively
1995; Santorufo et al., 2012). Hence, mechanisms for excreting of excess small quantity of metal passes through the mid-gut into haemolymph,
trace metals from the body have evolved. which distributes the metal around the soma. Thus, the processes that
occur in the midgut epithelium are fundamental to the accumulation/ex-
4.5. Output of trace metals from arthropods cretion of trace metals. Trace metals retained in the midgut epithelia cells
can be easily excreted by shedding of the cells containing accumulated
Trace metals not assimilated will be expulsed from the body in undi- metals or by the secretory activity of the epithelia cells. Trace metals
gested food. For trace metals entering the cells of the mid-gut and asso- passing through the midgut may be expelled via excretory organs, such
ciated structures, the principal mechanism of excretion is via cellular as the malpighian tubules, or sequestered in other tissues from which ex-
processes. These include the shedding of degenerated/sloughed cells, cretion is difficult or impossible (for instance anthrocytes), leading to
or the extrusion of MRGs into the lumen of the alimentary canal or he- longer term retention and the potential for biomagnification into the
patopancreas by holocrine/apocrine secretion (Sohal et al., 1977; next trophic level.
Ludwig and Alberti, 1988; Dallinger, 1993; Vandenbulcke et al., 1998a;
Przybylowicz et al., 2003; Pigino et al., 2006; Barka, 2007). These mech- 5. Predatory arthropods
anisms can lead to the efficient excretion of trace metals from the body
(Hopkin, 1990; Posthuma et al., 1992; Hensbergen et al., 2000; van der 5.1. Uptake, availability, transport, transformation and output of trace
Fels-Klerx et al., 2016). However, some species retain MGRs and these metals
tend to accumulate, and potentially biomagnify trace metals (Hopkin
1990; Dallinger, 1993; van der Fels-Klerx et al., 2016). The general sites and mechanisms of trace metal uptake, availability,
The exact nature and efficacy of excretion mechanisms is species transport, transformation and outputs in predatory arthropods do not
specific (Janssen et al., 1991; Kramarz, 1999a and b). Even two closely appear to differ between herbivorous and predatory arthropods. Conse-
related species with apparently identical digestive systems in terms of quently, the major factor that separates the two trophic levels in terms
structure and physical function can utilise the same structures in differ- of trace metal accumulation is diet. For instance, herbivorous arthro-
ent ways, resulting in very different excretion rates and therefore con- pods tend to consume a small fraction of a plant, whilst predatory ar-
centration with the body (Hopkin, 1990a, b). thropods tend to consume most, if not all, of their prey. Moreover, the
For assimilated trace metals passing through the mid-gut, there is differing nature of the diets between the two trophic levels is likely to
experimental evidence that excretory/osmo-regulatory organs, such as be reflected in their digestive enzymes (Chapman, 1998). The form of
the malpighian tubules of insects, can remove trace metals from the trace metals in the food of predatory arthropods will also differ.
haemolymph and thence from the body (Donker et al., 1996; Martin However, the assimilation efficiencies between trophic levels do not dif-
et al., 2007). Evidence for this is most clear in the case of Zn. In larval fer markedly (Janssen et al., 1991), which may suggest that differences
D. melanogaster, ZIP71B/ZIP5 is expressed on the basolateral surface of in availability are compensated for by the efficacy of the digestive
the malpighian tubule cells, where it functions to influx Zn from the enzymes.
haemolymph (Yin et al., 2017). Several genes for the ZnT Zn efflux pro- The availability of metals in the food of predatory arthropods is un-
teins are reportedly expressed in the malpighian tubules (Lye et al., derstood to depend on the chemical form of the metal, principally
16
whether the metals are bound to proteins/peptides (MTs, ferritin, gluta- 5.2. Predatory arthropods and multi-trophic metal transfer
thione, enzymes, respiratory pigments, etc.) or MRGs (Laskowski and
Hopkin, 1996; Vijver et al., 2004). Protein bound metals, especially sol- The anatomy and physiology of predatory Arthropods does not differ
uble proteins such as MTs, are thought to be readily available to preda- dramatically from herbivorous Arthropods and thus it is not surprising
tors (Laskowski and Hopkin, 1996; Vijver et al., 2004). In contrast, that differences in metal accumulation do not commonly occur between
MRGs, by their very nature, are insoluble and as granule expulsion the two trophic levels. However, several factors will affect the accumu-
into the gut lumen appears to be an effective mechanism for excreting lation of metal within a predator. These are 1) the physiology of the
trace metals, metals do seem to be readily re-absorbed from MRGs. predator (i.e. does it excrete metals or store/detoxify them); 2) the
Hence, it seems that granules are poorly solubilised by digestive fluids metal concentration the prey; 3) the form of the metal within the
(Hopkin, 1989; Laskowski and Hopkin, 1996; Rainbow et al., 2006). prey (i.e. protein/peptide bound or in MRGs); 4) feeding mechanism;
However, the neogastropod mollusc Nassarius festivus can assimilate 5) whether it is a specific predator adapted to metal concentrations/
metals bound in MRGS (Rainbow et al., 2007). This could be related forms in its prey or a generalist with no adaptation; and 6) the level of
to the highly efficient digestive powers of this species, but the contamination in the ecosystem. From this, generalist, liquid feeding
same authors found that a model of the invertebrate digestive sys- predators that have prey species that poorly excrete metals and have
tem was also able to leach Cd and Zn from MRGs (Rainbow et al., a high proportion of metal bound to proteins would be the most vulner-
2007). Based on both experiments, metals bound to MT like proteins able to metal pollution as their high exposure could overwhelm their
were more available than those bound to MRGs (Rainbow et al., ability to excrete and/or detoxify the metal, further increasing the risk
2007). Overall, the majority of trace metals in a cell is expected to of biomagnification to their own predators.
be in chemical forms that can be absorbed by a predator (Vijver
et al., 2004). 6. Metal accumulation across trophic levels
Considering the above, the feeding mechanism of predatory arthro-
pods may be a key factor governing the uptake of trace metals 6.1. Accumulation strategies
(Hendrickx et al., 2003). This may be particularly important for Cd, as
it is primarily accumulated within the soft proteinaceous tissues in ar- Organisms tend to exhibit one of five strategies of metal accumu-
thropods (Hughes et al., 1980) and is particularly bound to MT in the lation on increasing exposure to trace metals: hyperregulator;
midgut (Marioni et al., 1986; Hensbergen et al., 2000). Arthropods accumulator-hyperregulator; accumulator-regulator; accumulator
that feed by injecting digestive enzymes into their prey and sucking and hyperaccumulator (Fig. 5). Here, we define exposure as both
out the resultant partially digested tissues may therefore be feeding an increase in dose level or duration of an increased dose, with accu-
on tissues in which both the concentration and availability of Cd are mulation strategies generally holding true under both situations.
high compared to the whole animal. Hyperregulators are able to maintain an almost constant concentra-
Experimental evidence suggests that predatory Arthropods that feed tion over a wide range of exposures. However, the physiological mecha-
by piercing and sucking, such as spiders, lacewing larvae and pseudo- nism underlying regulation can become overburdened at high exposure
scorpions, do accumulate higher concentrations of Cd (Green et al., and the concentrations can then increase, leading to toxicity. The shoots
2006; Hendrickx et al., 2003; Janssen et al., 1991; Kramarz, 1999a; of many plant species exhibit this type of response, as do some arthro-
Scheifler et al., 2002; Babczynska et al., 2011). However, Hopkin and pods (Gräff et al., 1997; Kramarz, 1999a).
Martin (1985) have shown that the spider Dysdera crocata did not as- Accumulator-hyperregulators exhibit an initial increase in concen-
similate Cd when fed highly contaminated woodlice. This species is a tration with increasing exposure, but further exposure results in a de-
specialist predator of isopods, and may therefore have been adapted crease in concentration within the organism. This strategy can be
to the high concentrations of trace metals in its prey (Hopkin and observed as metal dose increases in arthropods (Crommentuijn et al.,
Martin, 1985). Therefore, it cannot be generalised that all piercing- 1994), but is more commonly seen when invertebrates are exposed to
sucking predators assimilate high concentrations of Cd from their an elevated concentration over time (Bednarska et al., 2011), with
prey, especially when Cd accumulation patterns can diverge between around 40% of invertebrate species exhibiting this type of response
male and female individuals within the same species, as verified in the (Laskowski et al., 2010).
spider Agelena labyrinthica (Babczynska et al., 2011). Accumulator–regulators undergo an initial rise in concentration, but
Knowledge of how feeding mechanisms affect Zn transfer be- the physiology of the organism reacts to prevent further accumulation.
tween herbivore and predator arthropods is more limited. However, Both plants (Green et al., 2006) and arthropods (Janssen et al., 1991;
studies have shown similar Zn biomagnification in the piercing, Kramarz, 1999a, b) are reported to utilise this strategy. The fourth strat-
sucking predator Chrysoperla carnae and two predatory beetles that egy of accumulator, is initially similar to that shown by accumulator-
consume the whole aphid, larval Coccinella septempunctata and regulators, but the organisms do not show any sign of regulating trace
Bembidion lampros (Green et al., 2006; Green et al., 2003; Winder metal concentrations. Instead, concentration increases linearly with
et al., 1999; Dar et al., 2017). Thus, the feeding mechanism possibly
plays a more limited role in determining Zn accumulation in arthro-
pods. This is perhaps due to the large extent to which Zn is bound to
polypeptides/proteins, its even distribution in the soma and the
ready leaching of Zn from MRGs (Lindqvist et al., 1995; Rainbow
et al., 2007).
Copper can be incorporated into mineral granules (Hopkin, 1989)
and to strongly induce synthesis of and to be bound to MTs (Dallinger,
1995). Hence, it can show biomagnification intermediate between Cd
and Zn (Janssen and Hogervorst, 1993). However, some studies have in-
dicated that Cu is effectively regulated via excretion and is not
biomagnified (Crawford et al., 1995; Rabitsch, 1995; Babczynska et al.,
2011). Similarly, Ni does not appear to be effectively biomagnified in
predators (Cheruiyot et al., 2013), although data on the forms of Ni in
cells and transfer between trophic levels is currently insufficient to
draw conclusions. Fig. 5. Models of organismal accumulation/regulation of metals by exposure.
17
exposure. Again, both plants (Baker, 1981) and arthropods exhibit this Sterenborg et al., 2003; Sá et al., 2008; Green et al., 2010; Bednarska
strategy (Janssen et al., 1991; Kramarz, 1999a; Hendrickx et al., 2003). et al., 2019). The three accumulator strategies show a general increase
The final strategy, hyperaccumulation, is characterised by organisms in concentration with exposure (time). Thus, for a population all exposed
accumulating very high concentrations of trace metals even when ex- to the same level of contaminant, older individuals in a population will
posed to low concentrations. This is seen in some metallophyte plants, tend to have higher concentrations in their bodies than younger individ-
but has not been reported for Arthropods. However, it has been sug- uals. Variability will be greatest in populations exhibiting an accumulator-
gested that herbivorous arthropods can use accumulated trace metals hyperregulator type pattern, as few newly exposed individuals (juveniles
as an elemental defence against predators (Boyd and Wall, 2001). In- and immigrants to the contaminated site) can exhibit concentrations in
deed, increased Cu and Zn levels in Spodoptera exigua retarted the devel- excess of 10 times greater than the steady state concentration of individ-
opment and growth of predator Podisus maculiventris (Cheruiyot et al., uals exposed over longer periods (Bednarska et al., 2011).
2013). Consequently, there is a possible evolutionary driver for some The process of biomagnification within food chains (the increase in
species of arthropods to develop hyperaccumulating physiology, and the concentration of a substance in an organism compared to its food)
this warrants further investigation in areas of naturally occurring metal- is acknowledged as a rare occurrence and is not a general characteristic
liferous soils. of food chains (Janssen et al., 1993). However, it has been suggested that
For plants, accumulation is determined by the extent to which critical pathways may be formed in which biomagnification of trace
metals are transferred from roots to shoots. In the case of regulators, metals may endanger some components (van Straalen and Ernst,
an effective root-shoot barrier exists that prevents metals reaching the 1991). Due to a lack of research into the transfer of metals within food
pericycle of the root, which consequently restricts the metal pool avail- chains, the existence of such pathways remains mostly theoretical.
able for loading into the xylem for transport to the shoot. Whilst this However, a consideration of the accumulation patterns in Fig. 5 sup-
may protect photosynthetically active cells from the metabolic disrup- ports the view that critical pathways can exist, but these are likely to
tion caused by excessive metal concentrations, it also means that such be rare. Most obviously, food chains consisting of accumulators are
plants cannot use the metal binding/detoxification capacity of the going to result in biomagnification and this may well result in secondary
shoot. Thus, accumulator and hyperaccumulator plants can show in- toxicity to organisms in the upper trophic levels, especially generalist,
creased tolerance to trace metals despite increasing the translocation liquid feeding predators. However, the inclusion of a hyperregulator or
of metals to the shoot. The physiological mechanisms involved are accumulator-hyperregulator in the chain would effectively block
related to elevated loading of trace metal ions into the xylem due to in- metal transfer to higher trophic levels, preventing the formation of a
creased cell to cell mobility and/or increased activity (Vmax) of trans- critical pathway. In addition, in field conditions, the local habitat fea-
porters effluxing ions from the cytoplasm into the xylem apoplast tures (e.g. habitat edges) can influence multitrophic transfer of metals,
(Richau et al., 2009; Verbruggen et al., 2009). especially for non-essential elements such as Cd (Orlowski et al.,
In invertebrates, the dominant physiological processes deter- 2019). These factors may explain why critical pathways remain appar-
mining the accumulation strategy may be those involved in the ex- ently rare and elusive.
cretion of trace metals, as assimilation efficiencies show much less Indeed this can be seen in Table 1, where we have compiled different
variation between taxa (Janssen et al., 1991). Excretion rate itself is experiments reporting Cu, Cd, Ni and/or Zn transfer across multiple tro-
probably determined by several factors, the importance of each dif- phic levels (in the field or in controlled environments), from soils to
fering among species. Species capable of regulating the concentra- plants, to herbivore arthropods and predator arthropods. Transfer coef-
tion of trace metals in their bodies (hyperregulators, accumulator- ficients can vary greatly (Table 1), depending the metal, organism and
hyperregulators, accumulator-regulators) most probably retain trophic level, however it is evident that a critical pathway (TC > 1) is
assimilated metal within the midgut, from where it can easily be rare to occur for all compartments involved (although it happens for
excreted. The excretory organs would also be a potential route for Zn in a few cases). It is also clear that studies which include all of the
excretion. However, it seems likely that this route would be sec- four compartments are lacking: predator arthropods and soils are less
ondary to processes in the midgut as trace metals entering the frequently reported (with herbivory being mainly the focus) from 27
haemolymph have the potential to be taken up by sensitive organs, studies, predators were absent in 12, whilst soil concentration values
hence transfer through the midgut is undesirable. were not included in seven of them (Table 1).
Accumulator arthropods largely retain metals within their bodies. One important point that cannot be overlooked when considering
Indeed, excretion can even be almost entirely absent even when ani- the potential for secondary toxicity is that very few species are monoph-
mals are returned to an uncontaminated diet (Janssen et al., 1991). agous and most species are therefore exposed to pollutants through
The physiological mechanisms underlying this behaviour are not clear, multiple pathways. In addition, arthopods are generally very good at
but may centre on the retention of metals in cells, tissues or organs lack- assessing the quality of their food, including the presence of elevated
ing openings to the outside (such as anthrocytes) or the repeated re- trace metals and can avoid or reduce the consumption of contaminated
absorption of metals excreted into the gut/excretory organ lumen. The food (Zidar et al., 2004; Bahadorani and Hilliker, 2009; Vesk and
evolution of a physiology that results in the retention of toxins seems Reichman, 2009; Green et al., 2010). Thus, in a food web, a predator
counter intuitive as invertebrates have a limited capacity to store trace may reduce the consumption of accumulator species and focus con-
metals in a detoxified state and when exceeded, soon suffer toxicity sumption on less contaminated prey. This may still affect the population
(Hopkin et al. 1990a; Crommentuijn et al., 1995). However, short of a species due to increased intraspecific competition for a reduced
lived species may be able to avoid the possible energetic and nutrient food source, which in turn could result in reduced reproductive output
costs of excretions (i.e. replacing shed cells) by limiting excretion whilst or survival. Hence, absence of trace metal accumulation does not neces-
having sufficient capacity to store/detoxify metals over their limited sarily mean an absence of effect.
life time.
7. Conclusions
6.2. Multitrophic transfer and biomagnification
Trace metals may occur in soils through natural and anthropogenic
The differences in accumulation strategies shed light on the behav- inputs and are generally retained within soils for long periods, typically
iour of trace metals within food chains, especially within the Arthropod in the most biologically active surface horizons (Adriano, 2001). The
components. Firstly, they help to explain the wide variation in trace major route by which trace metals can be transferred to organisms be-
metal concentrations reported in Arthropods, even under controlled yond the edaphic environment is through uptake by mycorrhizas and
laboratory conditions (Posthuma et al., 1992; Merrington et al., 2001; roots and their subsequent transfer to the above-ground biomass. The
18
Table 1
Total metal concentrations (M) and transfer coefficients (TC) of Cd, Cu, Ni and Zn within and between consecutive trophic levels: soil-plant-herbivorous arthropod-predatory arthropods.⁎
Compartment Setting Duration Obs. Ref.
Soil Plant Herbivore Predator
[M] Species [M] TC Species [M] TC Species [M] TC
Zn: 30.7 Triticum Zn: 18.8 Sitobion avenae Zn: 112 Bembidion Zn: 112 Zn: 1 F/C Plant: decimal Sewage sludge [1]
aestivum lampros stage 61–62 amended soil
Predator: 9 d
x Streptanthus Ni: 2900 x Melanotrichus Ni: 780 Ni: 0.27 Pholcus Ni: 470 Ni: 0.6 C Predator feed: Ni in [2]
polygatoides boydi phalangioides 33 d plant/herbivore is
assumed from
previous research
Cd: 0.12 Triticum Cd: 1.5 Cd: 13 Rhopalosiphum Cd: 2.9 Cd: 1.9 Mallada signata Cd: x Cd: x C Plant: [3]
Zn: 2.3 aestivum Zn: 57 Zn: 25 padi Zn: 324 Zn: 5.7 Zn: 41 Zn: 0.1 tillering + 22 d
Feed 1: 22 d
Feed 2: 12 d
Cu: 58.6 Forest litter Cu: 24.5 Cu: 0.4 Orchesella Cu: 6.2 Cu: 0.3 Pardosa sp. Cu: 13 Cu: 2.1 F x Invertebrates [4]
Ni: 43.1 (Salix, Ni: 43.1 Ni: 1.0 cincta Ni: x Ni: x Ni: x Ni: x sampled in the
Zn: 276 Carpinus) Zn: 122 Zn: 0.4 Zn: 79.3 Zn: 0.7 Zn: 197 Zn: 2.5 same field site
x x x x Fruit flies Cd: 54.5 x Pirata piraticus Cd: 142 Cd: 2.6 C 70 d Fruit flies fed in [5]
medium with
CdCl2
Cd: 0.5 Hordeum Cd: 0.22 Cd: 0.4 Sitobion avenae Cd: 0.36 Cd: 1.6 Chrysoperla Cd: 0.55 Cd: 1.5 C Plant: tillering Sewage sludge [6]
Zn: 91 vulgare Zn: 143 Zn: 1.6 Zn: 188 Zn: 1.3 carnae Zn: 249 Zn: 1.3 Feed 1: 10 d amended soil
Feed 2: 11 d
Cd: 0.16 Pisum sativum Cd: 0.15 Cd: 0.9 Acyrthosiphon Cd: 0.07 Cd: 0.5 x x x F Feeding: 72 d [7]
Zn: 32.5 Zn: 70 Zn: 2.2 pisum Zn: 135 Zn: 1.9
x Berkheya Cu: 10 x Anoplocnemis Cu: 65 Cu: 6.5 x x x F x [8]
coddii Ni: 16,000 curvipes Ni: 500 Ni: 0.03
Zn: 71 Zn: 180 Zn: 2.5
x Berkheya Cu: 10 x Chrysolina Cu: 100 Cu: 10 x x x F x [8]
coddii Ni: 16,000 clathrata Ni: 250 Ni: 0.02
Zn: 71 Zn: 150 Zn: 2.1
x Berkheya Cu: 10 x Stenoscepa sp. Cu: 45 Cu: 4.5 x x x F x [8]
coddii Ni: 16,000 Ni: 3500 Ni: 0.22
Zn: 71 Zn: 220 Zn: 3.1
x Sebertia Ni: 6900 x Bactrocera Ni: 65 Ni: 0.01 x x x F x Adult (larvae) [9]
acuminata psidii (420) (0.06) concentrations
x Berkheya Cu: 15 x Stenoscepa sp. Cu: 51 Cu: 3.4 x x x C 6d [10]
coddii Ni: 11,000 Ni: 3000 Ni: 0.3
Zn: 78 Zn: 430 Zn: 5.5
x Berkheya Cu: 2.3 x Chrysolina Cu: 47 Cu: 20.4 Rhinocoris Cu: 62 Cu: 1.3 F x Insects sampled in [11]
coddii Ni: 12,500 pardalina Ni: 1263 Ni: 0.1 neavii Ni: 516 Ni: 0.4 the same field site
Zn: 29 (larvae) Zn: 1080 Zn: 0.04 Zn: 362 Zn: 0.3
Cd: 18.5 Triticum Cd: 10.5 Cd: 0.6 Rhopalosiphum Cd: 13.5 Cd: 1.3 Chrysoperla Cd: 1.0 Cd: 0.1 C Plant: 31 d Soil spiked with [12]
aestivum padi carnae Feed 1: 14 d CdCl2
Feed 2: 6 d
Cd: 8.4 Rumex Cd: 0.31 Cd: 0.04 Spodoptera Cd: 0.05 Cd: 0.2 x x x F/C Feeding: 6 d Paper includes [13]
Cu: 60 patientia Cu: 1.4 Cu: 0.02 litura Cu: 6.9 Cu: 4.9 metal transfer to
Zn: 793 × R. Zn: 8.4 Zn: 0.01 Zn: 70 Zn: 8.3 chickens
tianschanicus
Cd: 0.7 Triticum Cd: 1.2 Cd: 1.7 Sitobion avenae Cd: 0.15 Cd: 0.1 Coccinella Cd: 0.12 Cd: 0.8 C Plant: stage Predator conc. [14]
Zn: 100 aestivum Zn: 70 Zn: 0.7 Zn: 130 Zn: 1.9 septempunctata Zn: 93 Zn: 0.7 37–51 estimated from
Feed 1: 28 d daily mean
Feed 2: 15 d intake × 15
Cd: 100 Setaria viridis Cd: 15 Cd: 0.15 Locusta Cd: 108 Cd: 7.2 x x x F x [15]
migratoria
Cd: 0.37 Oryza sativa Cd: 2.7 Cd: 7.3 Nilaparvata Cd: 1.4 Cd: 0.5 x x x C x [16]
Cu: 19.3 Cu: 24 Cu: 1.2 lugens Cu: 25 Cu: 1.1
Zn: 72.3 Zn: 104 Zn: 1.4 Zn: 183 Zn: 1.8
Cd: 23 Rumex Cd: 10 vCd: 0.4 Acrida cinerea Cd: 6.0 Cd: 0.6 x x x F x Average values [17]
Cu: 76 dentatus Cu: 30 Cu: 0.4 Cu: 50 Cu: 1.7 from 5 sites
Zn: 1034 Zn: 300 Zn: 0.3 Zn: 330 Zn: 1.1
Cd: 1.7 Brassica Cd: 5.5 Cd: 3.2 Lipaphis erysimi Cd: 4.5 Cd: 0.8 Coccinella Cd: 2.5 Cd: 0.6 C Plants: 61 d Sewage sludge [18]
Zn: 98 juncea Zn: 210 Zn: 2.7 Zn: 250 Zn: 1.2 septempunctata Zn: 230 Zn: 0.9 Feed 1: 21 d amended soil
Feed 2:
pupation
Cd: 0.16 Morus alba Cd: 0.03 Cd: 0.2 Bombyx mori Cd: 0.02 Cd: 0.7 x x x C Plant: 90 d Control (soil + Cd [19]
(67) (6.5) (0.1) (5.1) (0.8) Feeding: 5 d (NO3)2)
Cd: 1.8 Grasses (L. Cd: 2.5 Cd: 1.4 “Soil fauna” Cd: 19 Cd: 7.6 x x x F x Soil fauna: several [20]
Cu: 15 perenne, P. Cu: 11 Cu: 0.7 Cu: 38 Cu: 3.5 taxonomic groups
Ni: 23 pratense, P. Ni: 12 Ni: 0.5 Ni: 35 Ni: 2.9
Zn: 165 pratensis) Zn: 104 Zn: 0.6 Zn: 740 Zn: 7.1
Cd: 0.8 Brassica Cd: 1.7 Cd: 2.1 Lipaphis erysimi Cd: 2.1 Cd: 1.3 Coccinella Cd: 1.5 Cd: 0.7 C Plants: 61 d, Fly ash amended [21]
Zn: 55 juncea Zn: 75 Zn: 1.4 Zn: 150 Zn: 2.0 septempunctata Zn: 190 Zn: 1.3 Feed 1: 21 d, soil
Feed 2:
(continued on next page)
19
Table 1 (continued)
Compartment Setting Duration Obs. Ref.
Soil Plant Herbivore Predator
[M] Species [M] TC Species [M] TC Species [M] TC
pupation
Cd: 2.6 Solanum Cd: 11 Cd: 4.2 Dysmicoccus Cd: 5.5 Cd: 0.5 Cryptolaemus Cd: 3.5 Cd: 0.6 C Plant: Soil spiked with [22]
melongena neobrevipes montrouzieri flowering, Feed CdCl2
1: 21 d
Feed 2:
pupation
Cd: 2.6 Solanum Cd: 11.5 Cd: 4.4 Dysmicoccus Cd: 5.9 Cd: 0.5 Cryptolaemus Cd: 3.8 Cd: 0.6 C Plant: flowering Soil spiked with [22]
lycopersicum neobrevipes montrouzieri Feed 1: 21 d CdCl2
Feed 2:
pupation
Cd: 1.6 Trifolium Cd: 5.9 Cd: 3.7 Sitobion avenae Cd: 5.4 Cd: 0.9 Coccinella Cd: 6.0 Cd: 1.1 F x Average values [23]
Zn: 1.7 alexandrinum Zn: 12.9 Zn: 7.6 Zn: 14.7 Zn: 1.1 septempunctata Zn: 43 Zn: 2.9 from 5 sites
Cd: 1.6 Trifolium Cd: 5.9 Cd: 3.7 Aiolopus Cd: 35 Cd: 5.9 x x x F x Average values [23]
Zn: 1.7 alexandrinum Zn: 12.9 Zn: 7.6 thalassinus Zn: 128 Zn: 9.9 from 5 sites
Cd: 4.0 Medicago Cd: 0.25 Cd: 0.06 Spodoptera Cd: 0.06 Cd: 0.2 x x x C Feed: 8 days [24]
Cu: 532 sativa Cu: 19.2 Cu: 0.04 exigua Cu: 14.3 Cu: 0.7
Ni: 35.4 Ni: 3.1 Ni: 0.08 Ni: 0.6 Ni: 0.2
Zn: 1948 Zn: 91.6 Zn: 0.05 Zn: 132 Zn: 1.4
Cd, Ni: 200 Solanum x x Dysmicoccus Cd: 30.6 x Cryptolaemus Cd: 4.4 Cd: 0.14 C Plant: flowering Soils spiked with [25]
melongena neobrevipes Ni: 31.5 montrouzieri Ni: 5.2 Ni: 0.17 Feed 1: 21 d metal solutions to
Feed 2: 200 mg kg−1
pupation
Cd, Ni, Solanum x x Dysmicoccus Cd: 30.6 x Cryptolaemus x x C Plant: flowering Soils spiked with [26]
Zn: 200 melongena neobrevipes Ni: 31.5 montrouzieri Feed 1: unclear metal solutions to
Zn: 33.2 Feed 2: 200 mg kg−1
pupation
x Brassica napus Cd: 1.8 x Oulema Cd: 2.7 Cd: 1.5 Coccinella Cd: 0.9 Cd: 0.6 F 30 d Uncontrolled [27]
Cu: 105 melanopus Cu: 40 Cu: 0.4 septempunctata Cu: 180 Cu: 4.5 diet/other feeding
Zn: 6.0 Zn: 1.5 Zn: 0.3 Zn: 3.9 Zn: 2.6 sources
⁎ Some data extracted from figures; [M] metal concentration in the compartment (mg kg−1); TC: transfer coefficient between compartment, values >1 indicate a critical pathway;
Durations: timeframe of the experiment, assessment or animal feeding. Setting, F – field experiment/sampling; C – controlled environment (glasshouse, laboratory); x: absent, inapplicable
or unclear information. In experiments with multiple concentrations assessed, preference was given to the highest in the initial compartments (soil or plant). Refs. [1] Winder et al., 1999;
[2] Boyd and Wall, 2001; [3] Merrington et al., 2001; [4] Van Straalen et al., 2001; [5] Hendrickx et al., 2003; [6] Green et al., 2006; [7] Green and Tibbett, 2008; [8] Boyd et al., 2006a; [9]
Boyd et al., 2006b; [10] Boyd et al., 2007; [11] Migula et al., 2007; [12] Alonso et al., 2009; [13] Zhuang et al., 2009; [14] Green et al., 2010; [15] Zhang et al., 2012; [16] Wan et al., 2014 [17]
Zhang et al., 2014; [18] Dar et al., 2015; [19] Zhou et al., 2015; [20] Chrzan, 2016; [21] Dar et al., 2017; [22] Wang et al., 2017a, 2017b; [23] Butt et al., 2018; [24] Garrouj et al., 2018; [25]
Sang et al., 2018; [26] Du et al., 2019; [27] Orlowski et al., 2019.
most labile trace metals in the soil to shoot pathway are Cd and Zn and The key factors in controlling the transfer of trace metals through the
this can result in the bioaccumulation of both metals in shoot tissues soil-plant-Arthropod system are the type of metal, species and location
(Sauerbeck, 1991). Cu and Ni are moderately labile and tend not to in which the metal occurs in the lower trophic level as this will govern
biomagnify, with the exception of Nickel hyperaccumulators (~400 spe- its fate and transfer to the higher trophic level (Green et al., 2010;
cies from 4 families) found in metalliferous soils (Jaffre et al., 2013). Laskowski and Hopkin, 1996). Regulation can occur in all compartments
These metals have very low transfer coefficients in the soil-plant sys- of the system (Fig. 1; Table 1). This is controlled by the variation in the
tem, which results in much lower concentrations in shoot tissues than physiochemical environment in the soil and the physiology of plants
in the soil. It is clear, however, that the plant plays a major role in regu- and Arthropods. Without knowledge of all compartments it is difficult
lating the transfer of metals from soil to Arthropod, and should not be to predict the formation of a critical pathway.
regarded as a neutral carrier. Our knowledge of the physiology of essential trace metals has im-
Metal trafficking and binding to ligands within the plant can af- proved markedly in recent years, but similar efforts are needed to de-
fect the availability of metals and hence their subsequent transfer velop our understanding of the physiology of non-essential elements,
to herbivorous Arthropods. At this trophic level biomagnification such as Cd and Ni. Further research is also required to develop a full un-
can occur in herbivorous arthropods (Merrington et al., 1997b; derstanding of how predator guild may affect trace metal transfer and
Devkota and Schmidt, 2001; Green et al., 2006; Green and Tibbett, biomagnification (especially under field or mesocosm conditions), as
2008; Dar et al., 2017). As with the plant, it seems the physiology well as more dose-response investigations in arthropods, involving
of the Arthropod is then crucial in determining biomagnification, both physiological and gene expression analyses. It is also fundamental
and that may also occur in predatory Arthropods (Janssen et al., to learn the effects that interacting factors have on trace metal transfer
1991; Hendrickx et al., 2003; Green et al., 2006; Orlowski et al., and toxicity. These include: 1) how stress placed on plants by herbivory
2019). Although biomagnification is not a general property of affects metal uptake and translocation in the plant; 2) how metal accu-
plant-Arthropod and Arthropod-Arthropod systems, where a food mulation in herbivores affects predation through alteration of prey pal-
chain consists of species that accumulate trace metals in sequence, atability/prey choice by the predator and 3) how stress caused by metal
a critical pathway can be formed, which could result in secondary accumulation interacts with other ecological/environmental stressors,
toxicity. The effects of trace metal toxicity can be lethal or sub- such as parasite infection, other pollutants (including interactions be-
lethal, such as loss of fecundity, which will affect entire communities tween different trace metals) and food scarcity, can affect fitness of ex-
and populations. Moreover, whilst populations can adapt to high posed arthropods.
levels of trace metal in their environment, this comes at the cost of As this review has demonstrated, greater research effort is needed to
a shorter life span, increased reproductive effort and decreased ge- deliver a more holistic assessment of ecosystem toxicity, in which
netic diversity (Posthuma et al., 1993). integrated studies across ecosystem compartments will be crucial to
20
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brevicornis (Muller) exposed to copper, zinc, nickel, cadmium, silver and mercury.
Ecotoxicology 16, 491–502.
The authors declare that they have no known competing financial Barka, S., Pavillon, J.F., Amiard, J.C., 2001. Influence of different essential and non-essential
interests or personal relationships that could have appeared to influ- metals on MTLP levels in the copepod Tirgriopus brevicornis. Compar. Biochem. Phys-
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29

The Transfer of Trace Metals in The Soil-Plant-Arthropod System 2021

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Science of the Total Environment 779 (2021) 146260

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

The transfer of trace metals in the soil-plant-arthropod system

• Cd, Cu, Zn and Ni are prevalent and la-

amount and type of adsorbing phases, pH, Eh) consequently affect

2.5. Rhizosphere soils: modiﬁcation of trace metal chemistry by plants

Compartment Setting Duration Obs. Ref.

Soil Plant Herbivore Predator

[M] Species [M] TC Species [M] TC Species [M] TC

(continued on next page)

Compartment Setting Duration Obs. Ref.

Soil Plant Herbivore Predator

[M] Species [M] TC Species [M] TC Species [M] TC

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