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

https://doi.org/10.1016/j.scitotenv.2021.146260Get rights and content

Highlights

  • Cd, Cu, Zn and Ni are prevalent and labile metal cations in food chains in terrestrial ecosystems.

  • Current evidence on trophic transfer of metals and its underlying mechanisms are reviewed

  • Compartment-based approach: metal transfer via trophic pathways are considered as a series of linked compartments

  • Plants play a major role in regulating the transfer of metals from soil to Arthropods

  • Biomagnification is not a general property of plant-arthropod and arthropod-arthropod systems

Abstract

Essential and non-essential trace metals are capable of causing toxicity to organisms above a threshold concentration. Extensive research has assessed the behaviour of trace metals in biological and ecological systems, but has typically focused on single organisms within a trophic level and not on multi-trophic transfer through terrestrial food chains. This reinforces the notion of metal toxicity as a closed system, failing to consider one trophic level as a pollution source to another; therefore, obscuring the full extent of ecosystem effects. Given the relatively 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-arthropod herbivore-arthropod predator). In particular, we consider the mechanisms by which trace metals are taken up by organisms, the forms and transformations that can occur within the organism and the consequences for trace metal availability to the next trophic level. The review focuses on four of the most prevalent metal cations in soil which are labile in terrestrial food chains: Cd, Cu, Zn and Ni. Current knowledge of the processes and mechanisms by which these metals are transformed and moved within and between trophic levels in the soil-plant-arthropod system are evaluated. We demonstrate that the key factors controlling the transfer of trace metals through the soil-plant-arthropod system are the form and location in which the metal occurs in the lower trophic level and the physiological mechanisms of each organism in regulating uptake, transformation, detoxification and transfer. The magnitude of transfer varies considerably depending on the trace metal concerned, as does its toxicity, and we conclude that biomagnification is not a general property of plant-arthropod and arthropod-arthropod systems. To deliver a more holistic assessment of ecosystem toxicity, integrated studies across ecosystem compartments are needed to identify critical pathways that can result in secondary toxicity across terrestrial food-chains.

Introduction

Trace metals in soils (metallic elements with typical concentrations of <1000 mg kg−1) can be divided into two groups based on their biological function. The first group of elements, including Cu, Zn and Ni, are essential for the correct functioning of organisms (Marschner, 2012). The second group of trace elements have no known function in biological systems (Kabata-Pendias, 2010; Alloway, 2012a). Cadmium belongs to the second group when considering terrestrial ecosystems (Smolders and Mertens, 2012), although a biological role for Cd has been reported in marine diatoms (Lane and Morel, 2000; Xu et al., 2008). Both essential and non-essential trace metals are capable of causing toxicity above a certain threshold concentration. Extensive research has assessed the behaviour of trace metals in biological and ecological systems (e.g. Kabata-Pendias, 2010; Adriano, 2001; Peralta-Videa et al., 2009; Hooda, 2010; Alloway, 2012a; Jan et al., 2015). However, much of this research has typically focused on single organisms within a trophic level and not on multi-trophic transfer through terrestrial food chains, despite some notable field research and reviews on this topic (Fritsch et al., 2012; Nica et al., 2012; Orlowski et al., 2019; Pilon-Smits, 2019). This reinforces the notion of metal toxicity as a closed system, failing to consider one trophic level as a pollution source to another; therefore, obscuring the full extent of its ecosystem effects. This holistic eco(system)toxicity concept needs addressing, and is the fundamental precept for this review, which we hope will underpin more integrated research efforts in the future.

In this review we address this knowledge gap, synthesising evidence on trophic transfers of metals and the underlying mechanisms in soil-plant-arthropod food-chains for four of the most prevalent and labile metal cations in terrestrial food chains (Cd, Cu, Zn and Ni). Only one previous review has considered metal transfers in terrestrial multi-trophic systems (Gall et al., 2015), but the authors took a much broader approach than we apply here, in terms of the number of metals and mammalian and human endpoints, and did not focus on the underpinning mechanisms. Given the relatively few studies that deal with the trophic transfer of metals and the large number of studies within each trophic level, 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-arthropod herbivore-arthropod predator). In each compartment we consider the input to the compartment, transport and transformations that occur in that compartment and its transfer to the next (higher trophic) compartment (Fig. 1). The mechanisms by which trace metals are taken up by organisms, the forms and transformations that can occur within the organism and the effect that this may have on trace metal availability to the next trophic level are also explored.

Metals are inevitably transferred from one lower (trophic) compartment to the next higher (tropic) compartment but the magnitude of transfer varies due to a complex interaction of chemical and physiological factors. The net effect of these factors can be expressed as biomagnification (bioaccumulation) factors or transfer coefficients. Transfer coefficients (TCs) are calculated by dividing the concentration in one compartment of the system by the concentration in the compartment below it (e.g. concentration in the arthropod divided by the concentration in the plant tissue) (Green et al., 2003; Green and Tibbett, 2008; Li et al., 2018). A transfer coefficient of less than one leads to the dilution of metal(s) in the higher compartment, and more than one such contiguous diluting transfer forms a benign pathway (Fig. 2). A coefficient greater than one leads to the concentration of metals in the higher compartment, and more than one such contiguous concentrating transfer forms a critical pathway (van Straalen and Ernst, 1991) (Fig. 2).

The overall aim of the review is to identify the key factors controlling the transfer and toxicity of trace metals in excess in the soil-plant-arthropod system by addressing four research questions:

  • 1.

    What determines the soil bioavailability of trace metals to plants?

  • 2.

    What are the physiological mechanisms that regulate uptake, transformation, accumulation and detoxification in plants and herbivorous and predatory Arthropods?

  • 3.

    How do interactions between soil, plants and arthropods determine the magnitude of transfer between trophic levels?

  • 4.

    How important is biomagnification in soil-plant-arthropod systems and what are the consequences where it occurs?

Section snippets

Soils

Potentially toxic trace elements are naturally present in soils, being residual to a lesser or greater extent from the parent material and other natural sources (e.g. volcano, wind dust, forest fires) (Oorts, 2012). Significant additions of some trace elements, including Cu, Ni, Cd and Zn have been made to many soils as a result of human activities, from common agricultural practices to direct industrial waste disposal (Alloway, 2012b). Since potentially toxic trace elements may be transferred

Terrestrial plants

Terrestrial plants have developed a range of mechanisms to assimilate trace metals from soil environments with widely differing physical and chemical characteristics. In this section we discuss the plant physiological processes that govern the uptake, transport, transformation and storage of metals in plant tissues. These include the influence of roots and their associated mycorrhizal fungi on metal availability in the rhizosphere, and the factors regulating transport, complexation and

Invertebrate herbivores

Invertebrate herbivory affects all terrestrial plant families, although the extent of herbivory will vary with the effectiveness of the plants defence mechanism (Kant et al., 2015), and can occur at a variety of stages in a plant's development and by a wide range of arthropod grazers. Indeed, the phylum Arthropoda consists of a diverse range of organisms, which is reflected in the diversity of trace metal concentrations found in the species of this phylum (Dar et al., 2019). This is the case

Uptake, availability, transport, transformation and output of trace metals

The general sites and mechanisms of trace metal uptake, availability, transport, transformation and outputs in predatory arthropods do not appear to differ between herbivorous and predatory arthropods. Consequently, the major factor that separates the two trophic levels in terms of trace metal accumulation is diet. For instance, herbivorous arthropods tend to consume a small fraction of a plant, whilst predatory arthropods tend to consume most, if not all, of their prey. Moreover, the differing

Accumulation strategies

Organisms tend to exhibit one of five strategies of metal accumulation on increasing exposure to trace metals: hyperregulator; accumulator-hyperregulator; accumulator-regulator; accumulator and hyperaccumulator (Fig. 5). Here, we define exposure as both an increase in dose level or duration of an increased dose, with accumulation strategies generally holding true under both situations.

Hyperregulators are able to maintain an almost constant concentration over a wide range of exposures. However,

Conclusions

Trace metals may occur in soils through natural and anthropogenic inputs and are generally retained within soils for long periods, typically in the most biologically active surface horizons (Adriano, 2001). The major route by which trace metals can be transferred to organisms beyond the edaphic environment is through uptake by mycorrhizas and roots and their subsequent transfer to the above-ground biomass. The most labile trace metals in the soil to shoot pathway are Cd and Zn and this can

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References (511)

  • B. Braeckman et al.

    Cadmium uptake and defense mechanism in insect cells

    Environ. Res.

    (1999)
  • T. Bramryd

    Long-term effects of sewage sludge application on the heavy metal concentrations in acid pine (Pinus sylvestris L.) forests in a climatic gradient in Sweden

    For. Ecol. Manage.

    (2013)
  • N. Burford et al.

    Identification of complexes containing glutathione with As(III), Sb(II), Cd(II), Hg(II), Ti(I), Pb(II) or Bi(III) by electrospray ionization mass spectrometry

    J. Inorg. Biochem.

    (2005)
  • R. Burke et al.

    Expression and localisation of the essential copper transporter DmATP7 in Drosophila neuronal and intestinal tissues

    Int. J. Biochem. Cell Biol.

    (2008)
  • F.J. Cabañero et al.

    Different cation stresses affect specifically osmotic root hydraulic conductance, involving aquaporins, ATPase and xylem loading of ions in Capsicum annuum L. plants

    J. Plant Physiol.

    (2007)
  • Y. Cao et al.

    Xylem-based long-distance transport and phloem remobilization of copper in Salix integra Thunb

    J. Hazard. Mater.

    (2020)
  • R. Carrillo-González et al.

    Mechanisms and pathways of trace element mobility in soils

    Adv. Agron.

    (2006)
  • S.H. Chen et al.

    Phosphate supply and arsenate toxicity in ectomycorrhizal fungi

    J. Basic Microbiol.

    (2007)
  • Y. Chen et al.

    Diversity in cadmium accumulation and resistance associated withvarious metallothionein genes (type III) in Phytolacca americana L

    Int. J. Biol. Macromol.

    (2018)
  • S. Clemens

    Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants

    Biochimie.

    (2006)
  • E.P. Colangelo et al.

    Put the metal to the petal: metal uptake and transport throughout plants

    Curr. Opin. Plant Biol.

    (2006)
  • D.E. Conners et al.

    Effects of glutathione depletion on copper cytotoxicity in oysters (Crassostrea viriginica)

    Aquat. Toxicol.

    (2000)
  • A. Craig et al.

    Experimental evidence for cadmium uptake via calcium channels in the aquatic insect Chironomus staegeri

    Aquat. Toxicol.

    (1999)
  • T. Crommentuijn et al.

    Sublethal sensitivity index as an ecotoxicity parameter measuring energy allocation under toxicant stress — application to cadmium in soil arthropods

    Ecotoxicol. Environ. Saf.

    (1995)
  • D.C. Adriano

    Trace Elements in Terrestrial Environments: Biogeochemistry, Bioavailability and Risks of Metals

    (2001)
  • G.A. Ahearn et al.

    Mechanisms of heavy-metal sequestration and detoxification in crustaceans: a review

    J. Compar. Physiol. B Biochem. Syst. Environ. Physiol.

    (2004)
  • I. Ahumada et al.

    Effect of biosolid application to Mollisol Chilean soils on the bioavailability of heavy metals (Cu, Cr, Ni, and Zn) as assessed by bioassays with sunflower (Helianthus annuus) and DGT measurements

    J. Soils Sed.

    (2014)
  • H.E. Allen et al.

    Bioavailability of Metals in Terrestrial Ecosystems: Importance of Partitioning for Bioavailability to Invertebrates, Microbes, and Plants

    (2001)
  • B.J. Alloway

    Sources of heavy metals and metalloids in soils

  • H. Amir et al.

    Arbuscular mycorrhizal fungi from New Caledonian ultramafic soils improve tolerance to nickel of endemic plant species

    Mycorrhiza.

    (2013)
  • M. Amyot et al.

    Total metal burdens in the freshwater amphipod Gammarus fasiatus: contribution of various body parts and influence of gut contents

    Freshw. Biol.

    (1996)
  • E. Andresen et al.

    Trace metal metabolism in plants

    J. Exp. Bot.

    (2018)
  • L. Andrzejewska et al.

    Distribution of heavy metal pollution in plants and herbivorous Spodoptera littoralis L. (Lepidoptera)

    Ekol. Pol.

    (1990)
  • M. Anju et al.

    Associations of cadmium, zinc, and lead in soils from a lead and zinc mining area as studied by single and sequential extractions

    Environ. Monit. Assess.

    (2011)
  • Y. Aoki et al.

    Excretion of cadmium and change in the relative ratio of iso-cadmium-binding proteins during metamorphosis of fleshfly (Sarcophaga peregrine)

    Comp. Biochem. Physiol.

    (1984)
  • P.T. Arnold et al.

    Comparative uptake kinetics and transport of cadmium and phosphate in Phleum pratense-Glomus deserticolum associations

    Environ. Toxicol. Chem.

    (1993)
  • C.A. Backes et al.

    Kinetics of cadmium and cobalt desorption from iron and manganese oxides

    Soil Sci. Soc. Am. J.

    (1995)
  • S. Bahadorani et al.

    Biological and behavioral effects of heavy metals in Drosophila melanogaster adults and larvae

    J. Insect Behav.

    (2009)
  • S. Bahadorani et al.

    A Drosophila model of Menkes disease reveals a role for DmATP7 in copper absorption and neurodevelopment

    Dis. Models Mech.

    (2010)
  • A.J.M. Baker

    Accumulators and excluders-strategies in the response of plants to heavy metals

    J. Plant Nutr.

    (1981)
  • D.E. Baker et al.

    Copper

  • K. Balamurugan et al.

    Copper homeostasis in Drosophila by complex interplay of import, storage and behavioral avoidance

    EMBO J.

    (2007)
  • D.I. Bannon et al.

    Effect of DMT1 knockdown on iron, cadmium and lead uptake in Caco-2 cells

    Am. J. Physiol. Cell Physiol.

    (2003)
  • S. Barka

    Insoluble detoxification of trace metals in a marine copepod Tigriopus brevicornis (Muller) exposed to copper, zinc, nickel, cadmium, silver and mercury

    Ecotoxicology

    (2007)
  • N.T. Basta et al.

    Trace element chemistry in residual-treated soil: key concepts and metal bioavailability

    J. Environ. Qual.

    (2005)
  • A.J. Bednarska et al.

    Effects of nickel and temperature on the ground beetle Pterostichus oblongopunctatus (Coleoptera: Carabidae)

    Ecotoxicology

    (2008)
  • A.J. Bednarska et al.

    Two-phase uptake of nickel in the ground beetle Pterostichus oblongopunctatus (Coleoptera: Carabidae): implications for invertebrate metal kinetics

    Arch. Environ. Contam. Toxicol.

    (2011)
  • A.J. Bednarska et al.

    Effects of cadmium bioavailability in food on its distribution in different tissues in the ground beetle Pterostichus oblongopunctatus

    Bull. Environ. Contam. Toxicol.

    (2019)
  • C.B.M. Begg et al.

    Root-induced iron oxidation and pH changes in the lowland rice rhizosphere

    New Phytol.

    (1994)
  • Cited by (27)

    • Toxic effect of Cd burden on the gut microflora and immune responses of wolf spider Pardosa pseudoannulata

      2023, Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology
    View all citing articles on Scopus
    View full text