CoChat
Sign Up
Cited by 13Environmental Toxicology and EcotoxicologyPhysiological and biochemical adaptationsCollembola Taxonomy and Ecology Studies

The DOI matches its Crossref record; the references it cites are not checked yet.

Copper-contaminated soil compromises thermal performance in the springtail Folsomia candida (Collembola)

Open access
Ge, Jian, Slotsbo, Stine, Sørensen, Jesper G., Holmstrup, Martin·2023·Science of The Total Environment
DOI 10.1016/j.scitotenv.2023.165334
Open this paper in CoChat — free accountOpen PDF

Abstract

The widespread agricultural and industrial emissions of copper-based chemicals have increased copper levels in soils worldwide. Copper contamination can cause a range of toxic effects on soil animals and influence thermal tolerance. However, toxic effects are commonly investigated using simple endpoints (e.g., mortality) and acute tests. Thus, how organisms respond to ecological realistic sub-lethal and chronic exposures across the entire thermal scope of an organism is not known. In this study, we investigated the effects of copper exposure on the thermal performance of a springtail (Folsomia candida), regarding its survival, individual growth, population growth, and the composition of membrane phospholipid fatty acids. Folsomia candida (Collembola) is a typical representative of soil arthropods and a model organism that has been widely used for ecotoxicological studies. In a full-factorial soil microcosm experiment, springtails were exposed to three levels of copper (ca. 17 (control), 436, and 1629 mg/kg dry soil) and ten temperatures from 0 to 30 °C. Results showed that three-week copper exposure at temperatures below 15 °C and above 26 °C negatively influenced the springtail survival. The body growth was significantly lower for the springtails in high-dose copper soils at temperatures above 24 °C. A high copper level reduced the number of juveniles by 50 %, thereby impairing population growth. Both temperature and copper exposure significantly impacted membrane properties. Our results indicated that high-dose copper exposure compromised the tolerance to suboptimal temperatures and decreased maximal performance, whereas medium copper exposure partially reduced the performance at suboptimal temperatures. Overall, copper contamination reduced the thermal tolerance of springtails at suboptimal temperatures, probably by interfering with membrane homeoviscous adaptation. Our results show that soil organisms living in copper-contaminated areas might be more sensitive to thermally stressful periods.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.scitotenv.2023.165334

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

The citation lists haven’t been fetched yet

References 80 · Cited by 13

Research works printed but not linked: 72

  1. Ardestani, 2013, Dynamic bioavailability of copper in soil estimated by uptake and elimination kinetics in the springtail Folsomia candida, Ecotoxicology, 22, 308, 10.1007/s10646-012-1027-8 · DOI
  2. Ardestani, 2014, Uptake and elimination kinetics of metals in soil invertebrates: a review, Environ. Pollut., 193, 277, 10.1016/j.envpol.2014.06.026 · DOI
  3. Aucoin, 1995, How do insect herbivores cope with the extreme oxidative stress of phototoxic host plants?, Arch. Insect Biochem. Physiol., 29, 211, 10.1002/arch.940290210 · DOI
  4. Bates, 2015, Fitting linear mixed-effects models using lme4, J. Stat. Softw., 67, 1, 10.18637/jss.v067.i01 · DOI · Paper page
  5. Bindesbøl, 2009, Changes in membrane phospholipids as a mechanistic explanation for decreased freeze tolerance in earthworms exposed to sublethal copper concentrations, Environ. Sci. Technol., 43, 5495, 10.1021/es900898y · DOI
  6. Boas, 2016, Increased frequency of freeze-thaw events in a future climate can significantly increase negative effects of copper on enchytraeids, Appl. Soil Ecol., 107, 272, 10.1016/j.apsoil.2016.06.011 · DOI
  7. Boiteau, 2012, Locomotor response of Folsomia candida (Collembola: Isotomidae) to cooling temperatures, Environ. Entomol., 41, 916, 10.1603/EN12008 · DOI
  8. Buch, 2016, Ecotoxicity of mercury to Folsomia candida and Proisotoma minuta (Collembola: Isotomidae) in tropical soils: baseline for ecological risk assessment, Ecotox Environ Safe, 127, 22, 10.1016/j.ecoenv.2016.01.009 · DOI
  9. Buckley, 2016, Temperature extremes: geographic patterns, recent changes, and implications for organismal vulnerabilities, Glob. Chang. Biol., 22, 3829, 10.1111/gcb.13313 · DOI
  10. Calap-Quintana, 2017, Drosophila melanogaster models of metal-related human diseases and metal toxicity, Int. J. Mol. Sci., 18, 1456, 10.3390/ijms18071456 · DOI
  11. Callahan, 2019, Effects of copper exposure and increased temperatures on Collembola in western Washington, USA, City and Environment Interactions, 4, 10.1016/j.cacint.2020.100026 · DOI
  12. Chamberlain, 2005, Fatty acid compositions of Collembola: unusually high proportions of C20 polyunsaturated fatty acids in a terrestrial invertebrate, Comp. Biochem. Physiol. B: Biochem. Mol. Biol., 140, 299, 10.1016/j.cbpc.2004.10.016 · DOI
  13. Cronan, 1975, Thermal regulation of the membrane lipid composition of Escherichia coli. Evidence for the direct control of fatty acid synthesis, J. Biol. Chem., 250, 7074, 10.1016/S0021-9258(19)41040-5 · DOI
  14. Delignette-Muller, 2015, fitdistrplus: an R package for fitting distributions, J. Stat. Softw., 64, 1, 10.18637/jss.v064.i04 · DOI
  15. Dowling, 1986, Phospholipid ester-linked fatty acid biomarkers of acetate-oxidizing sulphate-reducers and other sulphide-forming bacteria, Microbiology, 132, 1815, 10.1099/00221287-132-7-1815 · DOI
  16. Durães, 2018, Distribution, transport and fate of pollutants, Elsevier, 29
  17. Elkin, L.A., Kay, M., Higgins, J.J., Wobbrock, J.O., n.d. An Aligned Rank Transform Procedure for Multifactor Contrast Tests. ACM.https://doi.org/10.1145/3472749.3474784. · DOI
  18. Ernst, 2016, Homeoviscous adaptation and the regulation of membrane lipids, J. Mol. Biol., 428, 4776, 10.1016/j.jmb.2016.08.013 · DOI · Paper page
  19. Ferreira, 2015, Long-term exposure of the isopod Porcellionides pruinosus to nickel: costs in the energy budget and detoxification enzymes, Chemosphere, 135, 354, 10.1016/j.chemosphere.2015.04.025 · DOI · Paper page
  20. Formentini, 2015, Copper and zinc accumulation and fractionation in a clayey Hapludox soil subject to long-term pig slurry application, Sci. Total Environ., 536, 831, 10.1016/j.scitotenv.2015.07.110 · DOI
  21. Halliwell, 2015, Free radicals in biology and medicine, Oxford University Press, Oxford, UK.
  22. Haubert, 2008, Effects of temperature and life stage on the fatty acid composition of Collembola, Eur. J. Soil Biol., 44, 213, 10.1016/j.ejsobi.2007.09.003 · DOI
  23. Hazel, 1995, Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?, Annu. Rev. Physiol., 57, 19, 10.1146/annurev.ph.57.030195.000315 · DOI
  24. Hazel, 1990, The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment, Prog. Lipid Res., 29, 167, 10.1016/0163-7827(90)90002-3 · DOI
  25. Holmstrup, 2018, Combined effects of drought and cold acclimation on phospholipid fatty acid composition and cold-shock tolerance in the springtail Protaphorura fimata, J. Comp. Physiol. B., 188, 225, 10.1007/s00360-017-1127-0 · DOI
  26. Holmstrup, 2002, Drought acclimation and lipid composition in Folsomia candida: implications for cold shock, heat shock and acute desiccation stress, J. Insect Physiol., 48, 961, 10.1016/S0022-1910(02)00175-0 · DOI
  27. Holmstrup, 2008, Exposure to mercury reduces cold tolerance in the springtail Folsomia candida, Comp Biochem Phys C, 148, 172
  28. Holmstrup, 2010, Interactions between effects of environmental chemicals and natural stressors: a review, Sci. Total Environ., 408, 3746, 10.1016/j.scitotenv.2009.10.067 · DOI
  29. Janssen, 1991, The effect of temperature on cadmium kinetics and oxygen consumption in soil arthropods, Environ. Toxicol. Chem., 10, 1493, 10.1002/etc.5620101115 · DOI
  30. Järup, 2003, Hazards of heavy metal contamination, Br. Med. Bull., 68, 167, 10.1093/bmb/ldg032 · DOI · Paper page
  31. Jegede, 2017, Temperature influences the toxicity of deltamethrin, chlorpyrifos and dimethoate to the predatory mite Hypoaspis aculeifer (Acari) and the springtail Folsomia candida (Collembola), Ecotox Environ Safe, 140, 214, 10.1016/j.ecoenv.2017.02.046 · DOI
  32. Jensen, 2016, National monitoring study in Denmark finds increased and critical levels of copper and zinc in arable soils fertilized with pig slurry, Environ. Pollut., 214, 334, 10.1016/j.envpol.2016.03.034 · DOI
  33. Jørgensen, 2022, Extreme escalation of heat failure rates in ectotherms with global warming, Nature, 611, 93, 10.1038/s41586-022-05334-4 · DOI
  34. Kozlov, 2007, Industrial barrens: extreme habitats created by non-ferrous metallurgy, Rev. Environ. Sci. Biotechnol., 6, 231, 10.1007/s11157-006-9117-9 · DOI
  35. Kwak, 2016, Trophic transfer of silver nanoparticles from earthworms disrupts the locomotion of springtails (Collembola), J. Hazard. Mater., 315, 110, 10.1016/j.jhazmat.2016.05.005 · DOI
  36. Lamichhane, 2018, Thirteen decades of antimicrobial copper compounds applied in agriculture. A review, Agronomy for Sustainable Development, 38, 10.1007/s13593-018-0503-9 · DOI
  37. Laskowski, 2010, Interactions between toxic chemicals and natural environmental factors - a meta-analysis and case studies, Sci. Total Environ., 408, 3763, 10.1016/j.scitotenv.2010.01.043 · DOI
  38. Lindquist, 1986, The heat-shock response, Annu. Rev. Biochem., 55, 1151, 10.1146/annurev.bi.55.070186.005443 · DOI
  39. Liu, 2020, Effects of decreasing temperature on phospholipid fatty acid composition of different tissues and hematology in Atlantic salmon (Salmo salar), Aquaculture, 515, 10.1016/j.aquaculture.2019.734587 · DOI
  40. Los, 2004, Membrane fluidity and its roles in the perception of environmental signals. Biochimica et Biophysica Acta (BBA), Biomembranes, 1666, 142, 10.1016/j.bbamem.2004.08.002 · DOI · Paper page
  41. Mallard, 2020, From individuals to populations: how intraspecific competition shapes thermal reaction norms, Funct. Ecol., 34, 669, 10.1111/1365-2435.13516 · DOI
  42. Maraldo, 2006, Effects of copper on enchytraeids in the field under differing soil moisture regimes, Environ. Toxicol. Chem., 25, 604, 10.1897/05-076R.1 · DOI
  43. Maria, 2014, Oxidative stress biomarkers and metallothionein in Folsomia candida - responses to Cu and Cd, Environ. Res., 133, 164, 10.1016/j.envres.2014.05.027 · DOI
  44. Martin, 2007, Regulation of long chain unsaturated fatty acid synthesis in yeast, Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1771, 271, 10.1016/j.bbalip.2006.06.010 · DOI
  45. Masindi, 2018, Environmental contamination by heavy metals, Heavy metals, 10, 115
  46. McBride, 2009, A comparison of tests for extractable copper and zinc in metal-spiked and field-contaminated soil, Soil Sci., 174, 10.1097/SS.0b013e3181b66856 · DOI
  47. Mikami, 2003, Membrane fluidity and the perception of environmental signals in cyanobacteria and plants, Prog. Lipid Res., 42, 527, 10.1016/S0163-7827(03)00036-5 · DOI
  48. Naveed, 2014, Simultaneous loss of soil biodiversity and functions along a copper contamination gradient: when soil goes to sleep, Soil Sci. Soc. Am. J., 78, 1239, 10.2136/sssaj2014.02.0052 · DOI
  49. Neaman, 2020, Analyzing soil metal toxicity: spiked or field-contaminated soils?, Environ. Toxicol. Chem., 39, 513, 10.1002/etc.4654 · DOI
  50. Niehaus, 2012, Predicting the physiological performance of ectotherms in fluctuating thermal environments, J. Exp. Biol., 215, 694, 10.1242/jeb.058032 · DOI
  51. Nursita, 2005, The effects of cadmium, copper, lead, and zinc on the growth and reproduction of Proisotoma minuta Tullberg (Collembola), Ecotox Environ Safe, 60, 306, 10.1016/j.ecoenv.2004.05.001 · DOI
  52. Padfield, 2021, rTPC and nls.multstart: a new pipeline to fit thermal performance curves in r, Methods Ecol. Evol., 12, 1138, 10.1111/2041-210X.13585 · DOI
  53. Pedersen, 1999, The impact of a copper gradient on a microarthropod field community, Ecotoxicology, 8, 467, 10.1023/A:1008964021344 · DOI
  54. Rahmstorf, 2011, Increase of extreme events in a warming world, Proc. Natl. Acad. Sci., 108, 17905, 10.1073/pnas.1101766108 · DOI
  55. Rath, 2015, Salt effects on the soil microbial decomposer community and their role in organic carbon cycling: a review, Soil Biol. Biochem., 81, 108, 10.1016/j.soilbio.2014.11.001 · DOI
  56. Schmalensee, 2021, Thermal performance under constant temperatures can accurately predict insect development times across naturally variable microclimates, Ecol. Lett., 24, 1633, 10.1111/ele.13779 · DOI
  57. Schneider, 2012, NIH image to ImageJ: 25 years of image analysis, Nat. Methods, 9, 671, 10.1038/nmeth.2089 · DOI · Paper page
  58. Scott-Fordsmand, 1997, Sublethal toxicity of copper to a soil-dwelling springtail (Folsomia fimetaria) (Collembola: Isotomidae), Environ. Toxicol. Chem., 16, 2538, 10.1002/etc.5620161215 · DOI
  59. Scott-Fordsmand, 2000, Responses of Folsomia fimetaria (Collembola: Isotomidae) to copper under different soil copper contamination histories in relation to risk assessment, Environ. Toxicol. Chem., 19, 1297, 10.1002/etc.5620190511 · DOI
  60. Sechi, 2014, Collembola feeding habits and niche specialization in agricultural grasslands of different composition, Soil Biol. Biochem., 74, 31, 10.1016/j.soilbio.2014.02.019 · DOI
  61. Sinensky, 1974, Homeoviscous adaptation—a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli, Proc. Natl. Acad. Sci., 71, 522, 10.1073/pnas.71.2.522 · DOI
  62. Smolders, 2009, Toxicity of trace metals in soil as affected by soil type and aging after contamination: using calibrated bioavailability models to set ecological soil standards, Environ. Toxicol. Chem., 28, 1633, 10.1897/08-592.1 · DOI
  63. Sørensen, 1995, The effects of sublethal dimethoate exposure on the locomotor behavior of the collembolan Folsomia candida (Isotomidae), Environ. Toxicol. Chem., 14, 1587, 10.1002/etc.5620140919 · DOI
  64. Sørensen, 2003, The evolutionary and ecological role of heat shock proteins, Ecol. Lett., 6, 1025, 10.1046/j.1461-0248.2003.00528.x · DOI
  65. Spurgeon, 1995, Extrapolation of the laboratory-based OECD earthworm toxicity test to metal-contaminated field sites, Ecotoxicology, 4, 190, 10.1007/BF00116481 · DOI
  66. Tranvik, 1993, Relative abundance and resistance traits of two Collembola species under metal stress, The Journal of Applied Ecology, 30, 43, 10.2307/2404269 · DOI
  67. Valko, 2005, Metals, toxicity and oxidative stress, Curr. Med. Chem., 12, 1161, 10.2174/0929867053764635 · DOI · Paper page
  68. Villeneuve, 2021, Environment and phenology shape local adaptation in thermal performance, Proc. R. Soc. B Biol. Sci., 288
  69. Waagner, 2013, Induced cold-tolerance mechanisms depend on duration of acclimation in the chill-sensitive Folsomia candida (Collembola), J. Exp. Biol., 216, 1991
  70. Wobbrock, J.O., Findlater, L., Gergle, D., Higgins, J.J., n.d. The aligned rank transform for nonparametric factorial analyses using only ANOVA procedures. ACM. https://doi.org/10.1145/1978942.1978963. · DOI
  71. Xu, 2009, Evaluation of growth and reproduction as indicators of soil metal toxicity to the Collembolan, Sinella curviseta, Insect Science, 16, 57, 10.1111/j.1744-7917.2009.00254.x · DOI
  72. Xu, 2009, Effects of copper, lead and zinc in soil on egg development and hatching of Folsomia candida, Insect Science, 16, 51, 10.1111/j.1744-7917.2009.00253.x · DOI

Metadata

Authors
Ge, J., Slotsbo, S., Sørensen, J. G., & Holmstrup, M.
Affiliations
Aarhus University (DK)
Corresponding author
Ge, Jian
ORCID
Venue
Science of The Total Environment
Publisher
Elsevier BV
Published
2023-11
Volume
897
Pages
165334
ISSN
0048-9697 (ISSN-L)
DOI
10.1016/j.scitotenv.2023.165334
OpenAlex
W4383376005
Cited by
13
References
80
Citations by year
2026: 4 · 2025: 1 · 2024: 6 · 2023: 1
FWCI
1.38
Type
journal article
Language
en
Open access
Licence
Locations
  • The Science of The Total Environment (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Horizon 2020
  • H2020 Marie Skłodowska-Curie Actions
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
  • Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Collembola Taxonomy and Ecology Studies
Keywords
copper contamination, Folsomia candida, Collembola, heat tolerance, thermal performance, soil microcosms, soil arthropods, homeoviscous adaptation, physical growth, population growth, survival, temperature stress
MeSH terms
Animals, Arthropods, Copper, Environmental Pollution, Reproduction, Soil, Soil Pollutants

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review