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Life in a Contaminated Environment: How Soil Nematodes Can Indicate Long-Term Heavy-Metal Pollution Cover

Life in a Contaminated Environment: How Soil Nematodes Can Indicate Long-Term Heavy-Metal Pollution

Open Access
|Nov 2022

Figures & Tables

Figure 1

Map of selected localities: (A) control meadows situated 3.6 km before pollution source; (B) meadow near waste sedimentation pond; (C) meadow near the heap of mine waste situated 680 m from (B); and (D) meadows near old bakery mill situated 3.7 km from (B) and (E) meadow close to village Jince situated 13.3 km from the pollution source.

Table 1

Soil physico- chemical properties (mean ± SD) associated with alluvial meadows in the vicinity of the Příbram mine along the Litavka River.

ABCDE
pH/KCl6.89 ± 0.25a5.42 ± 0.21a5.20 ± −0.11b5.56 ± 0.16b6.75 ± 0.18a
Soil moisture (%)35.2 ± 5.6a31.5 ± 2.9a29.5 ± 3.1a30.5 ± 3.3a31.5 ± 2.8a
Ntot (%)0.87 ± 0.15a0.61 ± 0.10b0.74 ± 0.32b0.66 ± 0.15b0.83 ± 0.22a
Cox (%)14.25 ± 1.69a8.25 ± 2.19b10.67 ± 3.61b12.29 ± 2.69a12.87 ± 3.16a

[i] Means followed by the same letters on the same rows are not statistically different by Tukey's honestly significant difference (HSD) at p < 0.05, n = 4.

Table 2

Total concentrations of heavy metals (mg/kg) (mean ± SD) associated with alluvial meadows in the vicinity of the Příbram mine along the Litavka River.

ABCDE
As38.2 ± 3.3a688.8 ± 91.8c677.4 ± 181.1c176.2 ± 47.7b31.8 ± 17.8a20
Cd1.9 ± 0.2a19.5 ± 1.9b51.5 ± 23.1c28.4 ± 12.9bc2.1 ± 1.0a0.5
Cr37.9 ± 5.1a58.2 ± 1.3b68.8 ± 59.9a40.4 ± 5.7a28.7 ± 1.7a90
Cu35.7 ± 5.3a97.6 ± 8.7b139.6 ± 24.6c61.9 ± 30.7ab23.1 ± 11.9a60
Ni19.1 ± 1.3a38.1 ± 2.4b33.2 ± 8.2ab22.9 ± 8.3a15.4 ± 1.8a50
Pb553.3 ± 237.6a3734.1 ± 1915.6b4030.9 ± 165.1bc2682.2 ± 460.3b689.8 ± 474.3a60
Zn346.2 ± 34.6a2949.5 ± 435.9b6867.8 ± 1374.9c3866.4 ± 1146.2b566.4 ± 490.1a120

[i] Means followed by the same letters on the same rows are not statistically different by Tukey's honestly significant difference (HSD) at p < 0.05, n = 4.

Max – limits posted by The Decree of the Ministry of Land Management of the Czech Republic No. 437/2016 on the admissible values of harmful substances in uncontaminated soil.

Table 3

Total nematode abundance, number of genera, nematode community indices associated with alluvial meadows in the vicinity of the Příbram mine along the Litavka River (mean ± SD).

IndicesABCDE
Nematode abundance2193.2 ± 358.9a595.8 ± 130.9b513.8 ± 122.3b974.9 ± 340.4b1674.1 ± 263.5a
Genera number31.8 ± 1.7a25.8 ± 1.5b27.5 ± 5.1a21.5 ± 3.1b30.5 ± 4.2a
Maturity Index2.68 ± 0.12a2.12 ± 0.09b2.20 ± 0.10b2.22 ± 0.21b2.63 ± 0.15a
Maturity Index (2-5)2.89 ± 0.07a2.33 ± 0.16b2.37 ± 0.15b2.33 ± 0.19b2.85 ± 0.22a
Plant Parasitic Index2.69 ± 0.11a2.80 ± 0.18a2.88 ± 0.04a2.77 ± 0.14a2.73 ± 0.16a
Diversity Index (H´gen)3.49 ± 0.15a2.13 ± 0.25b2.47 ± 0.26b2.22 ± 0.18b3.09 ± 0.10a
Channel Index8.8 ± 4.0a23.0 ± 11.8b36.4 ± 12.9b30.9 ± 6.6b22.9 ± 19.6ab
Basal Index16.6 ± 2.3a32.9 ± 8.3b33.9 ± 10.7b33.7 ± 4.6b19.9 ± 9.3a
Enrichment Index71.5 ± 4.4a53.2 ± 10.9b50.3 ± 11.5b37.9 ± 16.2b66.7 ± 10.1b
Structure Index72.0 ± 3.2a44.5 ± 18.7b49.8 ± 13.1b47.9 ± 16.2b73.8 ± 12.3a
Total biomass, mg7.5 ± 1.2a2.1 ± 1.2b1.9 ± 1.3b4.9 ± 2.9b8.6 ± 2.5a

[i] Means followed by the same letters on the same rows are not statistically different by Tukey's honestly significant difference at P < 0.05, n = 4.

Figure 2

RDA biplot of prevailing nematode genera and heavy metals contents in the five alluvial meadows along the Litavka River in the vicinity of the Příbram mine pollution sources. (A) a control meadow 3.6 km upstream of the source of pollution; (B) meadow near waste sedimentation pond; (C) meadow near the heap of mine waste situated 680 m from (B); and (D) meadows near old bakery mill situated 3.7 km from (B) and (E) meadow close to village Jince situated 13.3 km from the pollution source. Amplimer = Amplimerlinius; Acrobelo = Acrobeloides; Aphelench = Aphelenchoides; Aporcela = Aporcelaimellus; Crassolb = Crassolabium; Criconem = Criconemoides; Dipttherp = Diptherophora; Eucephal = Eucephalobus; Eudoryla = Eudorylaimus; Eumonhys = Eumonhystera; Helicotl = Helicotylenchus; Hemicycl = Hemicycliophora; Heterocp = Heterocephalobus; Mesodorl = Mesodorylaimus; Mesorhab = Mesorhabditis; Paratyln = Paratylenchus; Pratylech = Pratylenchoides; Prismatl = Primatolaimus; Teratocep = Teratocepahlobus; Trichodr = Trichodorus; Tylenchr = Tylenchorhynchus. RDA, redundancy analysis.

Table 4

A abundance of nematode genera (mean ± SD) associated with alluvial meadows in the vicinity of the Příbram mine along the Litavka River.

Genus/trophic groupc-pABCDE
Bacterivores
Mesorhabditis1251.6 ± 103.424.3 ± 13.022.6 ± 14.25.3 ± 8.324.8 ± 14.5
Plectus2241.3 ± 44.123.9 ± 20.710.5 ± 2.90.9 ± 0.515.4 ± 2.8
Rhabditis1187.0 ± 63.921.8 ± 17.75.9 ± 1.29.5 ± 11.626.3 ± 10.8
Acrobeloides2143.3 ± 75.172.1 ± 8.415.4 ± 7.951.1 ± 26.640.5 ± 35.6
Cephalobus2123.5 ± 61.012.1 ± 8.95.9 ± 3.99.6 ± 10.223.2 ± 18.7
Eucephalobus253.3 ± 27.812.2 ± 9.320.5 ± 10.822.5 ± 15.911.6 ± 10.1
Prismatolaimus351.1 ± 60.812.1 ± 7.97.0 ± 3.311.9 ± 17.517.6 ± 5.3
Bunonema127.4 ± 14.9---2.2 ± 4.4
Eumonhystera226.2 ± 24.14.6 ± 5.95.0 ± 2.4-4.4 ± 8.7
Heterocephalobus218.3 ± 5.64.5 ± 3.4-8.6 ± 3.9-
Alaimus49.1 ± 18.10.6 ± 1.14.3 ± 7.3-12.2 ± 9.8
Bastiania38.7 ± 5.92.1 ± 4.22.6 ± 1.91.9 ± 3.84.6 ± 9.3
Anaplectus28.0 ± 5.41.9 ± 1.4---
Cervidellus27.9 ± 15.8--8.1 ± 6.647.0 ± 12.8
Teratocephalus32.3 ± 4.61.4 ± 2.99.5 ± 2.61.9 ± 3.810.3 ± 5.9
Eudiplogaster21.5 ± 3.00.5 ± 1.0-1.9 ± 3.82.3 ± 4.6
Acrobeles2---1.9 ± 3.816.8 ± 11.5
Amphidelus4--1.9 ± 3.8--
Ceratoplectus2-1.1 ± 2.32.2 ± 2.5--
Diploscapter1-1.4 ± 1.7--2.2 ± 4.4
Euteratocephalus2-4.0 ± 3.83.0 ± 2.0--
Chiloplacus2---2.9 ± 3.78.6 ± 10.6
Panagrolaimus1-1.0 ± 2.1--2.2 ± 4.4
Prodesmodora3-1.5 ± 2.0---
Wilsonema2-15.4 ± 14.8-1.9 ± 2.112.4 ± 8.3
Fungivores
Dorylaimoides4104.9 ± 59.4----
Aphelenchoides2113.6 ± 54.27.9 ± 5.98.2 ± 6.69.5 ± 11.539.6 ± 7.8
Aphelenchus224.4 ± 37.320.9 ± 12.32.1 ± 3.011.9 ± 6.22.2 ± 4.4
Ditylenchus212.5 ± 15.49.3 ± 7.66.5 ± 3.02.9 ± 5.93.2 ± 6.5
Diptheropthora310.9 ± 14.95.0 ± 5.08.5 ± 4.56.2 ± 2.86.0 ± 4.2
Tylencholaimus45.4 ± 6.34.2 ± 8.3--7.6 ± 10.2
Tylencholaimellus44.5 ± 9.10.5 ± 1.0---
Paraphelenchus2-1.2 ± 2.5--1.6 ± 3.2
Omnivores
Eudorylaimus491.1 ± 61.53.0 ± 3.90.9 ± 0.92.9 ± 3.753.1 ± 38.5
Mesodorylaimus476.2 ± 26.6---4.4 ± 8.7
Oxydirus560.5 ± 40.20.8 ± 1.6--1.6 ± 3.2
Dorylaimus424.3 ± 40.70.5 ± 1.02.4 ± 1.8-1.6 ± 3.2
Aporcelaimellus513.9 ± 16.41.0 ± 2.12.0 ± 1.43.8 ± 4.121.1 ± 6.9
Pungentus410.7 ± 12.60.4 ± 0.80.5 ± 1.0-4.9 ± 5.7
Achromadora33.1 ± 6.1----
Crassolabium41.5 ± 3.06.7 ± 6.31.5 ± 1.91.9 ± 1.2-
Axonchium5-2.8 ± 5.7---
Discolaimium4-2.1 ± 4.2---
Microdorylaimus4--0.5 ± 1.19.5 ± 11.4-
Paractinolaimus5-0.4 ± 0.8---
Predators
Tripyla37.7 ± 9.12.9 ± 5.9-1.9 ± 3.8-
Mononchus47.3 ± 9.00.5 ± 1.03.4 ± 2.1--
Prionchulus46.2 ± 8.7---1.6 ± 2.1
Clarkus43.1 ± 6.10.9 ± 1.08.0 ± 4.68.1 ± 5.014.4 ± 9.8
Mylonchulus43.1 ± 6.23.7 ± 5.91.1 ± 2.1-17.3 ± 14.6
Nygolaimus5----2.2 ± 4.4
Plant parasites
Helicotylenchus3163.8 ± 82.938.7 ± 31.160.9 ± 21.685.7 ± 64.8118.0 ± 57.6
Heterodera357.9 ± 47.431.8 ± 2.427.8 ± 17.378.6 ± 21.852.3 ± 134.8
Pratylenchoides336.9 ± 30.15.0 ± 1.2---
Malenchus250.9 ± 52.79.2 ± 2.55.8 ± 2.495.5 ± 21.92.2 ± 4.4
Rotylenchus329.3 ± 31.7-0.5 ± 1.10.9 ± 1.9-
Geocenamus327.0 ± 20.367.7 ± 47.062.5 ± 16.353.8 ± 4.422.4 ± 16.6
Gracilacus226.6 ± 12.939.8 ± 33.0--7.0 ± 13.9
Filenchus215.3 ± 12.05.1 ± 4.70.9 ± 1.94.3 ± 3.39.2 ± 10.6
Tylenchorhynchus314.7 ± 12.023.9 ± 27.13.9 ± 5.1-4.9 ± 5.7
Meloidogyne37.5 ± 8.210.7 ± 26.2-20.5 ± 14.599.6 ± 33.9
Tylenchus26.8 ± 9.90.8 ± 1.60.5 ± 1.11.9 ± 3.8-
Coslenchus26.1 ± 12.22.8 ± 3.7--2.3 ± 4.6
Amplimerlinius33.0 ± 6.11.3 ± 2.0---
Lelenchus22.6 ± 5.3--3.8 ± 7.6-
Criconemoides3----9.7 ± 7.0
Hemicycliophora3--105.7 ± 49.2303.1 ± 63.3195.3 ± 110.3
Longidorus5-3.4 ± 4.3--23.8 ± 8.2
Mesocriconema3--1.6 ± 2.1-15.6 ± 12.1
Paratrichodorus4-4.1 ± 1.5--24.9 ± 30.2
Paratylenchus2-27.0 ± 16.233.3 ± 10.823.4 ± 9.7177.1 ± 159.5
Pratylenchus3-31.6 ± 8.445.1 ± 14.1107.1 ± 28.9122.8 ± 40.2
Trichodorus4-4.3 ± 5.9--20.5 ± 18.4
Xenocriconemella3-4.3 ± 7.2---
Aglenchus2---3.9 ± 2.5-
Boleodorus2--2.8 ± 3.5--
Psilenchus2--1.1 ± 1.2--
Insect parasites
Steinernema1--2.8 ± 5.73.8 ± 4.4
Table 5

Mean (±SD) abundance of nematode trophic groups and functional guilds associated with alluvial meadows in the vicinity of the Příbram mine along the Litavka River.

ABCDE
Bacterivores1160.6 ± 604.5a218.6 ± 56.3b115.6 ± 44.9b139.9 ± 56.8b284.3 ± 119.9b
Ba1466.1 ± 142.5a48.5 ± 31.2b28.4 ± 18.3b14.8 ± 10.2b57.6 ± 30.0b
Ba2623.3 ± 149.5a152.3 ± 41.3b61.9 ± 8.3b109.3 ± 54.1b182.3 ± 78.9b
Ba362.1 ± 60.6a17.1 ± 13.8b19.1 ± 15.3b15.7 ± 25.1b32.3 ± 27.2ab
Ba49.1 ± 18.1a0.6 ± 1.1b0.6 ± 1.1b-10.0 ± 11.7a
Predators87.6 ± 79.38.8 ± 6.812.4 ± 9.810.1 ± 6.137.1 ± 14.8
P37.7 ± 9.2a2.9 ± 5.8a2.9 ± 5.8a1.9 ± 3.8a-
P419.5 ± 12.1a5.1 ± 5.0b12.4 ± 9.8a8.1 ± 5.0a33.3 ± 10.8a
P560.4 ± 40.2a0.8 ± 1.6b--3.8 ± 4.5b
Fungivores276.1 ± 196.9a49.0 ± 26.7b25.3 ± 7.6b30.6 ± 10.9b60.6 ± 24.8b
Fu2150.3 ± 39.8a39.4 ± 15.1b16.8 ± 7.9b24.3 ± 7.1b46.6 ± 31.4b
Fu310.9 ± 14.9a5.0 ± 5.0a8.5 ± 7.9a6.2 ± 6.5a6.0 ± 8.2a
Fu4114.8 ± 46.3a4.6 ± 8.0b4.6 ± 8.0b-7.6 ± 10.2b
Omnivores220.7 ± 167.4a17.2 ± 6.6b7.9 ± 3.0b18.1 ± 19.0b85.0 ± 44.3ab
Om33.0 ± 6.1----
Om4203.6 ± 90.0a12.7 ± 10.1b5.9 ± 3.7b14.3 ± 14.7b63.9 ± 40.6b
Om514.0 ± 6.4a4.3 ± 5.0b2.0 ± 2.4b3.8 ± 4.4b21.1 ± 5.6a
Plant parasites451.8 ± 117.5a299.7 ± 66.9a351.4 ± 98.0a782.5 ± 260.8a893.8 ± 249.3a
Pp2108.3 ± 52.5a84.6 ± 40.5a44.4 ± 25.7b187.3 ± 121.4a397.7 ± 262.4a
Pp3340.1 ± 15.7a206.1 ± 67.4a308.0 ± 84.9a589.2 ± 206.3a540.5 ± 111.2a
Pp4-8.4 ± 6.7--45.5 ± 35.8
Pp5-3.4 ± 4.3--23.8 ± 28.9

[i] Means followed by the same letters on the same rows are not statistically different by Tukey’s HSD at P < 0.05, n = 4.

Ba1,2,3,4 bacterivores; Fu2,3,4 fungivores; P3,4,5 predators; Om3,4,5 omnivores; Pp2,3,4,5 plant parasites.

HSD, honestly significant difference.

Figure 3

Plots of enrichment vs. structure indices associated with investigated alluvial meadows along the Litavka River contaminated by heavy metals in the vicinity of the Příbram mine pollution sources. A – control; (B) meadow near waste sedimentation pond; (C) meadow near the heap of mine waste situated 680 m from (B); and (D) meadows near old bakery mill situated 3.7 km from (B) and (E) meadow close to village Jince situated 13.3 km from the pollution source.

Figure 4

Functional metabolic footprints of nematode associated with investigated alluvial meadows along the Litavka River contaminated by heavy metals in the vicinity of the Příbram mine pollution sources. The vertical axis of each footprint represents the enrichment footprint and the horizontal axis represents the structural footprint. The x-axis coordinates of the metabolic footprint are calculated as SI – 0.5Fs/k and SI + 0.5Fs/k, where Fs is the sum of standardized C utilization by structure indicator taxa. The y-axis coordinates are calculated as EI – 0.5Fe/k and EI + 0.5 Fe/k, where Fe is the sum of standardized C utilization by enrichment indicator taxa. The functional metabolic footprint is depicted by sequentially joining points: SI – 0.5 Fs/k, EI; SI, EI + 0.5 Fe/k; SI + 0.5 Fs/k, EI; SI, EI – 0.5 Fe/k; and SI – 0.5 Fs/k, EI. A – control; (B) meadow near waste sedimentation pond; (C) meadow near the heap of mine waste situated 680 m from (B); and (D) meadows near old bakery mill situated 3.7 km from (B) and (E) meadow close to village Jince situated 13.3 km from the pollution source.

Table 6

Spearman’s rank correlation coefficients between soil physico-chemical properties, heavy metals, and nematode parameters in the alluvial meadows in the vicinity of the Příbram mine along the Litavka River.

AsCdCrCuNiPbZnpH/KClNtotCoxSM
AbundanceNsnsnsnsns−0.862**−0.748**−0.659**nsnsns
No. generansnsnsnsnsns−0.451*nsnsnsns
Ba1−0.524*nsnsnsns−0.599*−0.482*nsnsnsns
Ba2−0.633**nsnsnsns−0.826**−0.859**0.467*0.561*nsns
Ba3−0.489*nsnsns0.442*−0.631**−0.745**nsnsns0.412*
Ba4nsnsnsnsns−0.455*nsnsnsnsns
P3−0.583*ns−0.409*−0.460*ns−0.741**−0.692**nsnsnsns
P4nsnsnsnsnsns−0.423*nsnsnsns
P5nsnsns−0.559*ns−0.699**−0.711**nsnsns0.431*
Fu2−0.507*nsnsnsns−0.853**−0.626**−0.492*nsnsns
Fu3nsnsnsns0.455*nsns−0.522*nsnsns
Fu4−0.625**nsns−0.474*ns−0.769**−0.834**−0.439*nsnsns
Om3nsnsnsnsnsnsnsnsnsnsns
Om4−0.569*nsnsnsns−0.845**−0.869**ns−0.422*nsns
Om5−0.725**nsnsnsns−0.766**−0.683**−0.426*−0.445*nsns
Pp2nsnsnsnsns−0.432*−0.457*nsnsnsns
Pp3nsnsns0.466*0.529*ns0.513*nsnsns0.436*
Pp4nsnsnsnsnsnsnsnsnsnsns
Pp5nsnsnsnsnsnsnsnsnsnsns
H´sppnsnsns−0.425*ns−0.722**−0.634**nsnsnsns
MInsnsnsnsns−0.584**−0.605**0.433*nsnsns
MI (2–5)nsnsnsnsnsns−0.552*nsnsnsns
PPInsnsnsnsnsnsnsnsnsnsns
CInsnsnsnsnsnsnsnsnsnsns
EInsnsnsnsns−0.439*nsnsnsnsns
SI−0.548*nsnsnsns−0.658**−0.742**nsnsnsns

[i] *P < 0.05; **P < 0.01.

CI, channel index; EI, enrichment index; MI, maturity index; PPI, plant-parasitic index; ns, not significant; SI, structure index.

DOI: https://doi.org/10.2478/jofnem-2022-0053 | Journal eISSN: 2640-396X | Journal ISSN: 0022-300X
Language: English
Submitted on: Apr 28, 2022
Published on: Nov 20, 2022
Published by: Society of Nematologists, Inc.
In partnership with: Paradigm Publishing Services
Publication frequency: 1 issue per year

© 2022 Marek Renčo, Andrea Čerevková, Jakub Hlava, published by Society of Nematologists, Inc.
This work is licensed under the Creative Commons Attribution 4.0 License.