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

Marek Renčo; Andrea Čerevková; Jakub Hlava

doi:10.2478/jofnem-2022-0053

Figures & Tables

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.

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.

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.

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.

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_

	As	Cd	Cr	Cu	Ni	Pb	Zn	pH/KCl	N_tot	C_ox	SM
Abundance	Ns	ns	ns	ns	ns	−0.862**	−0.748**	−0.659**	ns	ns	ns
No. genera	ns	ns	ns	ns	ns	ns	−0.451*	ns	ns	ns	ns
Ba₁	−0.524*	ns	ns	ns	ns	−0.599*	−0.482*	ns	ns	ns	ns
Ba₂	−0.633**	ns	ns	ns	ns	−0.826**	−0.859**	0.467*	0.561*	ns	ns
Ba₃	−0.489*	ns	ns	ns	0.442*	−0.631**	−0.745**	ns	ns	ns	0.412*
Ba₄	ns	ns	ns	ns	ns	−0.455*	ns	ns	ns	ns	ns
P₃	−0.583*	ns	−0.409*	−0.460*	ns	−0.741**	−0.692**	ns	ns	ns	ns
P₄	ns	ns	ns	ns	ns	ns	−0.423*	ns	ns	ns	ns
P₅	ns	ns	ns	−0.559*	ns	−0.699**	−0.711**	ns	ns	ns	0.431*
Fu₂	−0.507*	ns	ns	ns	ns	−0.853**	−0.626**	−0.492*	ns	ns	ns
Fu₃	ns	ns	ns	ns	0.455*	ns	ns	−0.522*	ns	ns	ns
Fu₄	−0.625**	ns	ns	−0.474*	ns	−0.769**	−0.834**	−0.439*	ns	ns	ns
Om₃	ns	ns	ns	ns	ns	ns	ns	ns	ns	ns	ns
Om₄	−0.569*	ns	ns	ns	ns	−0.845**	−0.869**	ns	−0.422*	ns	ns
Om₅	−0.725**	ns	ns	ns	ns	−0.766**	−0.683**	−0.426*	−0.445*	ns	ns
Pp₂	ns	ns	ns	ns	ns	−0.432*	−0.457*	ns	ns	ns	ns
Pp₃	ns	ns	ns	0.466*	0.529*	ns	0.513*	ns	ns	ns	0.436*
Pp₄	ns	ns	ns	ns	ns	ns	ns	ns	ns	ns	ns
Pp₅	ns	ns	ns	ns	ns	ns	ns	ns	ns	ns	ns
H´spp	ns	ns	ns	−0.425*	ns	−0.722**	−0.634**	ns	ns	ns	ns
MI	ns	ns	ns	ns	ns	−0.584**	−0.605**	0.433*	ns	ns	ns
MI (2–5)	ns	ns	ns	ns	ns	ns	−0.552*	ns	ns	ns	ns
PPI	ns	ns	ns	ns	ns	ns	ns	ns	ns	ns	ns
CI	ns	ns	ns	ns	ns	ns	ns	ns	ns	ns	ns
EI	ns	ns	ns	ns	ns	−0.439*	ns	ns	ns	ns	ns
SI	−0.548*	ns	ns	ns	ns	−0.658**	−0.742**	ns	ns	ns	ns

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_

	A	B	C	D	E
Bacterivores	1160.6 ± 604.5^a	218.6 ± 56.3^b	115.6 ± 44.9^b	139.9 ± 56.8^b	284.3 ± 119.9^b
Ba₁	466.1 ± 142.5^a	48.5 ± 31.2^b	28.4 ± 18.3^b	14.8 ± 10.2^b	57.6 ± 30.0^b
Ba²	623.3 ± 149.5^a	152.3 ± 41.3^b	61.9 ± 8.3^b	109.3 ± 54.1^b	182.3 ± 78.9^b
Ba₃	62.1 ± 60.6^a	17.1 ± 13.8^b	19.1 ± 15.3^b	15.7 ± 25.1^b	32.3 ± 27.2^ab
Ba₄	9.1 ± 18.1^a	0.6 ± 1.1^b	0.6 ± 1.1^b	-	10.0 ± 11.7^a
Predators	87.6 ± 79.3	8.8 ± 6.8	12.4 ± 9.8	10.1 ± 6.1	37.1 ± 14.8
P₃	7.7 ± 9.2^a	2.9 ± 5.8^a	2.9 ± 5.8^a	1.9 ± 3.8^a	-
P₄	19.5 ± 12.1^a	5.1 ± 5.0^b	12.4 ± 9.8^a	8.1 ± 5.0^a	33.3 ± 10.8^a
P₅	60.4 ± 40.2^a	0.8 ± 1.6^b	-	-	3.8 ± 4.5^b
Fungivores	276.1 ± 196.9^a	49.0 ± 26.7^b	25.3 ± 7.6^b	30.6 ± 10.9^b	60.6 ± 24.8^b
Fu₂	150.3 ± 39.8^a	39.4 ± 15.1^b	16.8 ± 7.9^b	24.3 ± 7.1^b	46.6 ± 31.4^b
Fu₃	10.9 ± 14.9^a	5.0 ± 5.0^a	8.5 ± 7.9^a	6.2 ± 6.5^a	6.0 ± 8.2^a
Fu₄	114.8 ± 46.3^a	4.6 ± 8.0^b	4.6 ± 8.0^b	-	7.6 ± 10.2^b
Omnivores	220.7 ± 167.4^a	17.2 ± 6.6^b	7.9 ± 3.0^b	18.1 ± 19.0^b	85.0 ± 44.3^ab
Om₃	3.0 ± 6.1	-	-	-	-
Om₄	203.6 ± 90.0^a	12.7 ± 10.1^b	5.9 ± 3.7^b	14.3 ± 14.7^b	63.9 ± 40.6^b
Om₅	14.0 ± 6.4^a	4.3 ± 5.0^b	2.0 ± 2.4^b	3.8 ± 4.4^b	21.1 ± 5.6^a
Plant parasites	451.8 ± 117.5^a	299.7 ± 66.9^a	351.4 ± 98.0^a	782.5 ± 260.8^a	893.8 ± 249.3^a
Pp₂	108.3 ± 52.5^a	84.6 ± 40.5^a	44.4 ± 25.7^b	187.3 ± 121.4^a	397.7 ± 262.4^a
Pp₃	340.1 ± 15.7^a	206.1 ± 67.4^a	308.0 ± 84.9^a	589.2 ± 206.3^a	540.5 ± 111.2^a
Pp₄	-	8.4 ± 6.7	-	-	45.5 ± 35.8
Pp₅	-	3.4 ± 4.3	-	-	23.8 ± 28.9

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

Parameter	Sites
	A	B	C	D	E
pH/KCl	6.89 ± 0.25^a	5.42 ± 0.21^a	5.20 ± −0.11^b	5.56 ± 0.16^b	6.75 ± 0.18^a
Soil moisture (%)	35.2 ± 5.6^a	31.5 ± 2.9^a	29.5 ± 3.1^a	30.5 ± 3.3^a	31.5 ± 2.8^a
N_tot (%)	0.87 ± 0.15^a	0.61 ± 0.10^b	0.74 ± 0.32^b	0.66 ± 0.15^b	0.83 ± 0.22^a
C_ox (%)	14.25 ± 1.69^a	8.25 ± 2.19^b	10.67 ± 3.61^b	12.29 ± 2.69^a	12.87 ± 3.16^a

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

Element	Sites					Max
	A	B	C	D	E
As	38.2 ± 3.3^a	688.8 ± 91.8^c	677.4 ± 181.1^c	176.2 ± 47.7^b	31.8 ± 17.8^a	20
Cd	1.9 ± 0.2^a	19.5 ± 1.9^b	51.5 ± 23.1^c	28.4 ± 12.9^bc	2.1 ± 1.0^a	0.5
Cr	37.9 ± 5.1^a	58.2 ± 1.3^b	68.8 ± 59.9^a	40.4 ± 5.7^a	28.7 ± 1.7^a	90
Cu	35.7 ± 5.3^a	97.6 ± 8.7^b	139.6 ± 24.6^c	61.9 ± 30.7^ab	23.1 ± 11.9^a	60
Ni	19.1 ± 1.3^a	38.1 ± 2.4^b	33.2 ± 8.2^ab	22.9 ± 8.3^a	15.4 ± 1.8^a	50
Pb	553.3 ± 237.6^a	3734.1 ± 1915.6^b	4030.9 ± 165.1^bc	2682.2 ± 460.3^b	689.8 ± 474.3^a	60
Zn	346.2 ± 34.6^a	2949.5 ± 435.9^b	6867.8 ± 1374.9^c	3866.4 ± 1146.2^b	566.4 ± 490.1^a	120

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)_

Indices	A	B	C	D	E
Nematode abundance	2193.2 ± 358.9^a	595.8 ± 130.9^b	513.8 ± 122.3^b	974.9 ± 340.4^b	1674.1 ± 263.5^a
Genera number	31.8 ± 1.7^a	25.8 ± 1.5^b	27.5 ± 5.1^a	21.5 ± 3.1^b	30.5 ± 4.2^a
Maturity Index	2.68 ± 0.12^a	2.12 ± 0.09^b	2.20 ± 0.10^b	2.22 ± 0.21^b	2.63 ± 0.15^a
Maturity Index (2-5)	2.89 ± 0.07^a	2.33 ± 0.16^b	2.37 ± 0.15^b	2.33 ± 0.19^b	2.85 ± 0.22^a
Plant Parasitic Index	2.69 ± 0.11^a	2.80 ± 0.18^a	2.88 ± 0.04^a	2.77 ± 0.14^a	2.73 ± 0.16^a
Diversity Index (H´gen)	3.49 ± 0.15^a	2.13 ± 0.25^b	2.47 ± 0.26^b	2.22 ± 0.18^b	3.09 ± 0.10^a
Channel Index	8.8 ± 4.0^a	23.0 ± 11.8^b	36.4 ± 12.9^b	30.9 ± 6.6^b	22.9 ± 19.6^ab
Basal Index	16.6 ± 2.3^a	32.9 ± 8.3^b	33.9 ± 10.7^b	33.7 ± 4.6^b	19.9 ± 9.3^a
Enrichment Index	71.5 ± 4.4^a	53.2 ± 10.9^b	50.3 ± 11.5^b	37.9 ± 16.2^b	66.7 ± 10.1^b
Structure Index	72.0 ± 3.2^a	44.5 ± 18.7^b	49.8 ± 13.1^b	47.9 ± 16.2^b	73.8 ± 12.3^a
Total biomass, mg	7.5 ± 1.2^a	2.1 ± 1.2^b	1.9 ± 1.3^b	4.9 ± 2.9^b	8.6 ± 2.5^a

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

Genus/trophic group	c-p	A	B	C	D	E
Bacterivores
Mesorhabditis	1	251.6 ± 103.4	24.3 ± 13.0	22.6 ± 14.2	5.3 ± 8.3	24.8 ± 14.5
Plectus	2	241.3 ± 44.1	23.9 ± 20.7	10.5 ± 2.9	0.9 ± 0.5	15.4 ± 2.8
Rhabditis	1	187.0 ± 63.9	21.8 ± 17.7	5.9 ± 1.2	9.5 ± 11.6	26.3 ± 10.8
Acrobeloides	2	143.3 ± 75.1	72.1 ± 8.4	15.4 ± 7.9	51.1 ± 26.6	40.5 ± 35.6
Cephalobus	2	123.5 ± 61.0	12.1 ± 8.9	5.9 ± 3.9	9.6 ± 10.2	23.2 ± 18.7
Eucephalobus	2	53.3 ± 27.8	12.2 ± 9.3	20.5 ± 10.8	22.5 ± 15.9	11.6 ± 10.1
Prismatolaimus	3	51.1 ± 60.8	12.1 ± 7.9	7.0 ± 3.3	11.9 ± 17.5	17.6 ± 5.3
Bunonema	1	27.4 ± 14.9	-	-	-	2.2 ± 4.4
Eumonhystera	2	26.2 ± 24.1	4.6 ± 5.9	5.0 ± 2.4	-	4.4 ± 8.7
Heterocephalobus	2	18.3 ± 5.6	4.5 ± 3.4	-	8.6 ± 3.9	-
Alaimus	4	9.1 ± 18.1	0.6 ± 1.1	4.3 ± 7.3	-	12.2 ± 9.8
Bastiania	3	8.7 ± 5.9	2.1 ± 4.2	2.6 ± 1.9	1.9 ± 3.8	4.6 ± 9.3
Anaplectus	2	8.0 ± 5.4	1.9 ± 1.4	-	-	-
Cervidellus	2	7.9 ± 15.8	-	-	8.1 ± 6.6	47.0 ± 12.8
Teratocephalus	3	2.3 ± 4.6	1.4 ± 2.9	9.5 ± 2.6	1.9 ± 3.8	10.3 ± 5.9
Eudiplogaster	2	1.5 ± 3.0	0.5 ± 1.0	-	1.9 ± 3.8	2.3 ± 4.6
Acrobeles	2	-	-	-	1.9 ± 3.8	16.8 ± 11.5
Amphidelus	4	-	-	1.9 ± 3.8	-	-
Ceratoplectus	2	-	1.1 ± 2.3	2.2 ± 2.5	-	-
Diploscapter	1	-	1.4 ± 1.7	-	-	2.2 ± 4.4
Euteratocephalus	2	-	4.0 ± 3.8	3.0 ± 2.0	-	-
Chiloplacus	2	-	-	-	2.9 ± 3.7	8.6 ± 10.6
Panagrolaimus	1	-	1.0 ± 2.1	-	-	2.2 ± 4.4
Prodesmodora	3	-	1.5 ± 2.0	-	-	-
Wilsonema	2	-	15.4 ± 14.8	-	1.9 ± 2.1	12.4 ± 8.3
Fungivores
Dorylaimoides	4	104.9 ± 59.4	-	-	-	-
Aphelenchoides	2	113.6 ± 54.2	7.9 ± 5.9	8.2 ± 6.6	9.5 ± 11.5	39.6 ± 7.8
Aphelenchus	2	24.4 ± 37.3	20.9 ± 12.3	2.1 ± 3.0	11.9 ± 6.2	2.2 ± 4.4
Ditylenchus	2	12.5 ± 15.4	9.3 ± 7.6	6.5 ± 3.0	2.9 ± 5.9	3.2 ± 6.5
Diptheropthora	3	10.9 ± 14.9	5.0 ± 5.0	8.5 ± 4.5	6.2 ± 2.8	6.0 ± 4.2
Tylencholaimus	4	5.4 ± 6.3	4.2 ± 8.3	-	-	7.6 ± 10.2
Tylencholaimellus	4	4.5 ± 9.1	0.5 ± 1.0	-	-	-
Paraphelenchus	2	-	1.2 ± 2.5	-	-	1.6 ± 3.2
Omnivores
Eudorylaimus	4	91.1 ± 61.5	3.0 ± 3.9	0.9 ± 0.9	2.9 ± 3.7	53.1 ± 38.5
Mesodorylaimus	4	76.2 ± 26.6	-	-	-	4.4 ± 8.7
Oxydirus	5	60.5 ± 40.2	0.8 ± 1.6	-	-	1.6 ± 3.2
Dorylaimus	4	24.3 ± 40.7	0.5 ± 1.0	2.4 ± 1.8	-	1.6 ± 3.2
Aporcelaimellus	5	13.9 ± 16.4	1.0 ± 2.1	2.0 ± 1.4	3.8 ± 4.1	21.1 ± 6.9
Pungentus	4	10.7 ± 12.6	0.4 ± 0.8	0.5 ± 1.0	-	4.9 ± 5.7
Achromadora	3	3.1 ± 6.1	-	-	-	-
Crassolabium	4	1.5 ± 3.0	6.7 ± 6.3	1.5 ± 1.9	1.9 ± 1.2	-
Axonchium	5	-	2.8 ± 5.7	-	-	-
Discolaimium	4	-	2.1 ± 4.2	-	-	-
Microdorylaimus	4	-	-	0.5 ± 1.1	9.5 ± 11.4	-
Paractinolaimus	5	-	0.4 ± 0.8	-	-	-
Predators
Tripyla	3	7.7 ± 9.1	2.9 ± 5.9	-	1.9 ± 3.8	-
Mononchus	4	7.3 ± 9.0	0.5 ± 1.0	3.4 ± 2.1	-	-
Prionchulus	4	6.2 ± 8.7	-	-	-	1.6 ± 2.1
Clarkus	4	3.1 ± 6.1	0.9 ± 1.0	8.0 ± 4.6	8.1 ± 5.0	14.4 ± 9.8
Mylonchulus	4	3.1 ± 6.2	3.7 ± 5.9	1.1 ± 2.1	-	17.3 ± 14.6
Nygolaimus	5	-	-	-	-	2.2 ± 4.4
Plant parasites
Helicotylenchus	3	163.8 ± 82.9	38.7 ± 31.1	60.9 ± 21.6	85.7 ± 64.8	118.0 ± 57.6
Heterodera	3	57.9 ± 47.4	31.8 ± 2.4	27.8 ± 17.3	78.6 ± 21.8	52.3 ± 134.8
Pratylenchoides	3	36.9 ± 30.1	5.0 ± 1.2	-	-	-
Malenchus	2	50.9 ± 52.7	9.2 ± 2.5	5.8 ± 2.4	95.5 ± 21.9	2.2 ± 4.4
Rotylenchus	3	29.3 ± 31.7	-	0.5 ± 1.1	0.9 ± 1.9	-
Geocenamus	3	27.0 ± 20.3	67.7 ± 47.0	62.5 ± 16.3	53.8 ± 4.4	22.4 ± 16.6
Gracilacus	2	26.6 ± 12.9	39.8 ± 33.0	-	-	7.0 ± 13.9
Filenchus	2	15.3 ± 12.0	5.1 ± 4.7	0.9 ± 1.9	4.3 ± 3.3	9.2 ± 10.6
Tylenchorhynchus	3	14.7 ± 12.0	23.9 ± 27.1	3.9 ± 5.1	-	4.9 ± 5.7
Meloidogyne	3	7.5 ± 8.2	10.7 ± 26.2	-	20.5 ± 14.5	99.6 ± 33.9
Tylenchus	2	6.8 ± 9.9	0.8 ± 1.6	0.5 ± 1.1	1.9 ± 3.8	-
Coslenchus	2	6.1 ± 12.2	2.8 ± 3.7	-	-	2.3 ± 4.6
Amplimerlinius	3	3.0 ± 6.1	1.3 ± 2.0	-	-	-
Lelenchus	2	2.6 ± 5.3	-	-	3.8 ± 7.6	-
Criconemoides	3	-	-	-	-	9.7 ± 7.0
Hemicycliophora	3	-	-	105.7 ± 49.2	303.1 ± 63.3	195.3 ± 110.3
Longidorus	5	-	3.4 ± 4.3	-	-	23.8 ± 8.2
Mesocriconema	3	-	-	1.6 ± 2.1	-	15.6 ± 12.1
Paratrichodorus	4	-	4.1 ± 1.5	-	-	24.9 ± 30.2
Paratylenchus	2	-	27.0 ± 16.2	33.3 ± 10.8	23.4 ± 9.7	177.1 ± 159.5
Pratylenchus	3	-	31.6 ± 8.4	45.1 ± 14.1	107.1 ± 28.9	122.8 ± 40.2
Trichodorus	4	-	4.3 ± 5.9	-	-	20.5 ± 18.4
Xenocriconemella	3	-	4.3 ± 7.2	-	-	-
Aglenchus	2	-	-	-	3.9 ± 2.5	-
Boleodorus	2	-	-	2.8 ± 3.5	-	-
Psilenchus	2	-	-	1.1 ± 1.2	-	-
Insect parasites
Steinernema	1	-	-	2.8 ± 5.7	3.8 ± 4.4

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

Figures & Tables

Figure 1

Figure 2

Figure 3

Figure 4

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_

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_

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

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

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)_

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

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