Terrestrial Non-Parasitic Nematode Assemblages associated With Glyphosate-tolerant and Conventional Soybean-Based Cropping Systems

Mbatyoti, Akhona; Daneel, Mieke Stefanie; Swart, Antoinette; de Waele, Dirk; Fourie, Hendrika

doi:10.21307/jofnem-2018-028

Figures & Tables

Location of the six localities where terrestrial, non-parasitic nematodes were sampled from soybean fields (2011/12: red triangles and 2012/13: blue triangles) and adjacent natural vegetation (yellow triangles) during two consecutive growing seasons (Map compiled by: Ms L. de Swart, NWU).

Canonical correspondence analyses (CCA) of population densities of terrestrial, non-parasitic nematode genera identified from 200 g soil samples obtained from three ecosystems: glyphosate-tolerant soybean fields, conventional soybean fields, and natural vegetation in Edenville during 2012/13 season.

(A and B) Faunal profiles (Sieriebriennikov et al., 2014) representing the enrichment and structural conditions of soil food webs on the abundance and diversity of terrestrial, non-parasitic nematode genera identified from soils of glyphosate-tolerant and conventional soybean fields, as well as adjacent natural vegetation sites (39 in total) sampled during 2011/12 and 2012/13 seasons (A) and data for such sites pooled for the two seasons (B) in South African soybean production areas.

Fig. 4

A faunal, soil food web profile representing the enrichment and structural indices (EI and SI, respectively) of terrestrial, non-parasitic nematode assemblages identified at the three sampling dates in glyphosate-tolerant and non-treated plot halves planted with soybean (during 2013/14 growing season) and maize (during 2014/15 growing season).

Prominence values (PV), mean population density (MPD) and frequency of occurrence (FO%) of non-parasitic nematode genera identified from 200 g soil samples from glyphosate-tolerant and conventional soybean fields, as well as natural vegetation from 28 sites in the soybean production area of South Africa during the 2011/12 and 2012/13 growing seasons_

Genus	PV	FO%	MPD	Genus	PV	FO %	MPD	Genus	PV	FO%	MPD
Glyphosate-tolerant soybean				Conventional soybean				Natural vegetation
2011/12 season
Aphelenchus	3,646	100	3,646	Panagrolaimus	2,723	75	3,144	Acrobeles	3,885	100	3,885
Acrobeles	2,131	50	3,014	Acrobeloides	1,963	50	2,804	Aphelenchus	3,741	75	4,320
Acrobeloides	982	50	1,403	Aphelenchus	1,683	50	2,380	Acrobeloides	2,758	75	3,185
Eucephalobus	668	25	1,335	Aphelencohides	840	25	1,680	Panagrolaimus	1,310	50	1,853
Aphelenchoides	572	25	1,144	Acrobeles	444	50	634	Eucephalobus	907	50	1,281
Psilenchus	452	25	905	Plectus	338	25	675	Rhabditis	648	50	915
Panagrolaimus	253	25	505	Cephalobus	216	25	431	Cephalobus	570	25	1,139
Rhabditis	197	25	393	Eucephalobus	171	25	342	Tylenchus	534	75	615
Mesorhabditis	168	25	335	Monhystera	158	25	315	Psilechus	184	50	262
Tylenchus	17	25	34	Mesorhabditis	130	25	259	Zeldia	71	25	142
Discolaimoides	3	25	5	Tylenchus	40	25	80	Dorylaimus	5	25	9
Thornenema	3	25	5	Psilenchus	20	25	40	Aporcellaimellus	4	25	8
Paraxonchium	2	25	4	Dorylaimus	4	25	7	Discolamium	3	25	5
–	–	–	–	Discolaimoides	3	25	5	Discolaimoides	2	25	3
–	–	–	–	Paraxonchium	2	25	3	–	–	–	–
–	–	–	–	Thornenema	2	25	3	–	–	–	–
2012/13 season
Aphelenchus	2,275	100	2,275	Aphelenchus	1,448	100	1,448	Aphelenchus	2,590	100	2,590
Acrobeles	1,230	89	1,304	Eucephalobus	988	44	1,490	Eucephalobus	2,425	83	2,662
Eucephalobus	941	78	1,065	Acrobeloides	821	67	1,003	Panagrolaimus	1,615	100	1,615
Acrobeloides	827	67	1,010	Panagrolaimus	553	33	962	Cephalobus	1,414	67	1,728
Rhabditis	824	67	1,007	Acrobeles	365	33	635	Acrobeloides	1,156	83	1,269
Aphelenchoides	781	56	1,043	Aphelenchoides	334	22	711	Acrobeles	849	56	1,134
Panagrolaimus	576	56	770	Seleborca	286	22	610	Aphelenhoides	817	67	998
Zeldia	298	33	519	Cephalobus	587	56	784	Ditylenchus	323	33	562
Cephalobus	148	22	315	Plectus	241	22	513	Plectus	183	33	319
Chiloplacus	63	11	190	Ditylenchus	212	22	451	Mesorhabditis	151	17	365
Ditylenchus	53	11	161	Mesorhabditis	206	33	439	Seleborca	77	17	186
Mesorhabditis	42	11	126	Plectus	201	22	429	Rhabditis	68	17	165
Plectus	34	11	108	Zeldia	98	11	295	Zeldia	66	17	159
Tylencholaimus	7	11	22	Chiloplacus	78	11	235	Wilsonema	65	17	157
Discolaimium	3	22	7	Dorylaimus	8	55	11	Chilopacus	63	17	154
Aporcelaimellus	3	22	6	Leptonchus	4	11	11	Teratocephalus	7	17	16
Eudorylaimus	2	11	7	Tylencholaimus	3	11	10	Eudorylaimus	7	33	12
Discolaimoides	2	11	6	Alaimus	3	11	9	Leptonchus	5	17	13
–	–	–	–	Mononchus	2	11	5	Coslenchus	4	17	10
–	–	–	–	–	–	–	–	Tylencholaimellus	4	17	9
–	–	–	–	–	–	–	–	Discolaimoides	3	17	8

Crop history, agricultural practices, fertilisers applied, glyphosate application dates, and dosage rate, nematode sampling dates, rainfall, and minimum and maximum temperatures recorded of the experimental plot during the 2013/14 and 2014/15 growing seasons_

Crop history: growing season, crop and herbicides applied	Growing season, crop and cultivar cultivated	Agricultural practice implemented	Inorganic fertiliser applied and dosage	Glyphosate application dates and dosage rates	Nematode sampling dates	Rainfall (mm)	Minimum temperature (°C)	Maximum temperature (°C)
2011/12, sunflower, no herbicide used (hand-hoeing of weeds)	2013/14 (1st year), soybean (cv. LS 6164 R)	Reap and plough before planting	None	10 January 2014 and 03 February 2014 @ 2 L/ha	1st = 30/01/2014;2nd = 14/02/2014;3rd = 22/04/2014	603	7.9	30.5
2012/13, maize, Gramoxone® (active substance bipyridyl 200 g/L as dichloride salt 276 g/L) dosage rate 3 L/ha	2014/15 (2nd year), maize (cv. DKC 80–30 RR)	Reap and plough before planting	2:3:2 (26) at planting @ 300 kg/ha Ureum @ 50 kg/ha 4 weeks after planting	17 December 2014 and 13 January 2015 @ 2 L/ha	1st = 08/01/2015;2nd = 27/01/2015;3rd = 11/03/2015	510	10.0	30.2

Non-parasitic nematodes genera mean population density data per 200 g rhizosphere soil of glyphosate-tolerant and conventional soybean crops, as well natural vegetation from 28 sites surveyed in the soybean production areas of South Africa during the 2011/12 and 2012/2013 growing seasons_ Values shown are means, followed by the standard deviation (SD)_

2011/12			2012/13
Ecosystems	t-value	P	Ecosystems	t-value	P
Acrobeles
Glyphosate-tolerant soybean: 603 ± 1,348Conventional soybean: 27 ± 284	0.15	0.88	Glyphosate-tolerant soybean: 261 ± 583Conventional soybean: 50 ± 335	0.06	0.97
Glyphosate-tolerant: 603 ± 1,348Natural vegetation: 777 ± 1,737	−0.02	0.98	Glyphosate-tolerant soybean: 261 ± 583 Natural veld: 227 ± 507	0.01	0.99
Conventional soybean: 127 ± 284Natural vegetation: 777 ± 1,737	−0.17	0.87	Conventional soybean: 150 ± 335 Natural veld: 227 ± 507	−0.04	0.97
Acrobeloides
Glyphosate-tolerant soybean: 281 ± 627Conventional soybean: 560 ± 1,254	0.06	0.96	Glyphosate-tolerant soybean: 202 ± 452Conventional soybean: 201 ± 449	0.001	1
Glyphosate-tolerant: 281 ± 627Natural vegetation: 637 ± 1,424	0.08	0.94	Glyphosate-tolerant: 202 ± 452Natural vegetation: 254 ± 568	0.02	0.98
Conventional soybean: 560 ± 1,254Natural vegetation: 637 ± 1,424	−0.01	0.99	Conventional soybean: 201 ± 449Natural vegetation: 254 ± 568	0.02	0.98
Aphelenchus
Glyphosate-tolerant soybean: 729 ± 1,631Conventional soybean: 476 ± 1,064	−0.04	0.97	Glyphosate-tolerant soybean: 455 ± 1,017Conventional soybean: 290 ± 648	0.04	0.97
Glyphosate-tolerant: 729 ± 1,631Natural vegetation: 864 ± 1,932	−0.12	0.91	Glyphosate-tolerant: 455 ± 1,017Natural vegetation: 518 ± 1,158	0.01	0.99
Conventional soybean: 476 ± 1,064Natural vegetation: 864 ± 1,932	−0.05	0.96	Conventional soybean: 290 ± 648Natural vegetation: 518 ± 1,158	0.05	0.96
Eucephalobus
Glyphosate-tolerant soybean: 267 ± 597Conventional soybean: 68 ± 153	−0.15	0.89	Glyphosate-tolerant soybean: 213 ± 476Conventional soybean: 298 ± 666	−0.03	0.97
Glyphosate-tolerant: 267 ± 597Natural vegetation: 256 ± 573	−0.004	1	Glyphosate-tolerant: 213 ± 476Natural vegetation: 532 ± 1,191	0.09	0.93
Conventional soybean: 68 ± 153Natural vegetation: 256 ± 573	−0.14	0.89	Conventional soybean: 298 ± 666Natural vegetation: 532 ± 1,191	0.05	0.96
Panagrolaimus
Glyphosate-tolerant soybean: 101 ± 226Conventional soybean: 629 ± 1,406	0.18	0.86	Glyphosate-tolerant soybean: 154 ± 344Conventional soybean: 192 ± 430	−0.02	0.98
Glyphosate-tolerant: 101 ± 226Natural vegetation: 371 ± 829	0.13	0.9	Glyphosate-tolerant: 154 ± 344Natural vegetation: 323 ± 722	0.07	0.94
Conventional soybean: 629 ± 1,406Natural vegetation: 371 ± 829	0.05	0.96	Conventional soybean: 192 ± 430Natural vegetation: 323 ± 722	0.05	0.96

Number of non-parasitic nematodes per 200 g rhizosphere soil of soybean cv_ LS 6164 R and maize cv_ DKC 80–30 RR plants in glyphosate-treated and non-treated small-field plot halves at three sampling dates during the 2013/14 and 2014/15 growing seasons_ Values shown are means, followed by the standard deviation (SD)_

		Soybean				Maize
Nematode genus	Functional guild, followed by c–p value	Glyphosate-treated	Non-treated	t-value	P	Glyphosate-treated	Non-treated	t-value	P
Acrobeles	Ba2	–	298 ± 527	−7	0.001	888 ± 1,029	–	−8.15	0.001
Acrobeloides	Ba2	201 ± 342	155 ± 172	0.9	0.37	1,001 ± 1,795	149 ± 169	−1.57	0.12
Aphelenchus	Fu2	475 ± 746	189 ± 249	0.31	0.76	2,635 ± 3,020	1,762 ± 2,002	−6.68	0.5
Aphelenchoides	Fu2	240 ± 394	–	5.25	0.001	1,226 ± 2,090	–	−4.15	0.001
Aporcelaimellus	Pr5	–	0.17 ± 1	−1	0.33	–	–
Cephalobus	Ba2	512 ± 1,011	189 ± 298	3.73	0.001	745 ± 1,098	256 ± 316	−0.96	0.34
Discolaimium	Pr5	–	0.22 ± 1	−0.99	0.33	–	–
Ditylenchus	Fu2	38 ± 92	–	3.16	0.002	–	–
Eucephalobus	Ba2	211 ± 407	46 ± 20	0.81	0.42	1,000 ± 1,129	89 ± 156	−3.98	0.001
Leptonchus	Fu4	10 ± 17	5 ± 13	1.54	0.13	–	–
Panagrolaimus	Ba2	544 ± 1,002	–	17.65	0.001	1,350 ± 1,542	267 ± 467	−3.41	0.001
Teratocephalus	Ba4	–	–	–	–	2 ± 7	16 ± 16	5.46	0.001
Tylenchus	Fu2	–	306 ± 537	−4.1	0.001	–	267 ± 462	4.16	0.001
Tylencholaimus	Fu4	5 ± 15	7 ± 17	−0.02	0.99	24 ± 35	12 ± 23	−2.76	0.007

Significance values (P and F-ratios) for three independent variables (ecosystem, locality, and season), according to a Mixed Models analysis, showing their effects (individually and in combination) on four non-parasitic nematode trophic groups that were identified in the soybean production areas of South Africa during the 2011/12 and 2012/13 growing seasons_

	Bacterivores		Fungivores		Omnivores		Predators
Source	F	P	F	P	F	P	F	P
Season	42.158	0.001**	17.322	0.001**	10.078	0.006**	4.531	0.049**
Ecosystem	0.489	0.622	0.536	0.595	0.675	0.523	6.384	0.009**
Season*Ecosystem	0.123	0.885	0.021	0.980	0.300	0.745	1.238	0.316
Locality	1.315	0.307	2.494	0.075	4.851	0.007**	8.648	0.001**
Season*Locality	1.073	0.388	3.540	0.039**	8.641	0.001**	24.999	0.001**
Ecosystem*Locality	0.580	0.794	0.930	0.526	0.554	0.814	2.001	0.108
SeasonEcosystemLocality	0.561	0.728	1.454	0.259	1.076	0.410	7.083	0.001**

Soybean cultivar planted at each soybean field, crop history, and selected soil chemical and physical properties of each field where plant-parasitic nematodes from roots and rhizosphere soil samples were collected during the 2011/12 and 2012/13 growing seasons_

				Soil chemical properties					Soil physical properties
Sampling season	Locality	Ecosystem and cultivar	Crop history	pH (H₂O)	Ca	Mg	K	Na	P	% Sand	% Silt	% Clay	% total C
2011/12 and 2012/13	Bothaville	Glyphosate-tolerant soybean (PAN1664R)	Maize/Sunflower	6.48	381	107	205	0.5	204	94.7	0.7	4.6	0.21
2012/13		Glyphosate-tolerant soybean (PAN1664R)	Maize/Sunflower	6.48	437	81	170	0.5	170	94.5	0.7	4.8	0.10
2011/12 and 2012/13		Conventional soybean (Egret)	Maize/Sunflower	6.89	581	81	246	1	166	92.6	0.7	6.7	0.23
2012/13		Conventional soybean (Egret)	Maize/Sunflower	6.43	374	96	203	0.5	203	94.6	0.7	4.7	0.22
2011/12 and 2012/13		Natural vegetation (grass)		6.77	446	78	194	0.5	169	94.5	0.7	4.7	0.21
2011/12 and 2012/13		Natural vegetation (grass)		6.06	574	165	400	5	252	89.6	3.4	7	1.5
2011/12 and 2012/13	Brits	Glyphosate-tolerant soybean (PAN1583R)	Maize/Sunflower	7.28	1,434	304	497	2	500	79.9	5.5	14.6	1.36
2011/12 and 2012/13		Conventional soybean (Egret)	Soybean/Wheat	7.49	1,699	346	291	58.5	399.	81.4	7.6	11	0.76
2011/12 and 2012/13		Natural vegetation (grass)		7.11	2,840	559	417	91.5	509	58.3	12.4	29.2	1.51
2011/12 and 2012/13		Natural vegetation (grass)		7.6	3,206	636	342	98	53	74.1	9.1	16.8	3.95
2012/13	Edenville	Glyphosate-tolerant soybean (PAN1664R)	Soybean	6.15	1,486	401	419	60.5	40	59.3	19.1	21.6	0.20
2012/13		Conventional soybean (Superboon)	Soybean	4.97	512	213	292	9.5	118	70.7	9.3	20	0.49
2012/13		Natural vegetation (grass)		5.92	396	67	268	3	93	85.9	3.4	10.7	3.89
2012/13		Natural vegetation (grass)		5.64	222	52	271	1.5	86	86.6	3.2	10.1	0.34
2011/12 and 2012/13	Marble Hall	Glyphosate-tolerant soybean (PAN1454R)	Maize/Soybean	6.09	666	228	390	20	402	84.9	6.7	8.4	0.56
2012/13		Glyphosate-tolerant soybean (LS6164R)	Maize/Soybean	6.64	541	149	146	23	118	91	3.7	5.1	0.84
2012/13		Glyphosate-tolerant soybean (LS6164R)	Maize/Soybean	6.07	826	212	291	176	336	88.7	3.7	7.6	0.40
2011/12 and 2012/13		Conventional soybean (Egret)	Soybean	7.05	1,001	402	390	34.5	67	78.6	8.7	12.7	0.58
2012/13		Conventional soybean (MC555)	Soybean	6.62	1,012	244	509	14.5	156	91.2	3.7	5.1	1.76
2011/12 and 2012/13		Natural vegetation (grass)		6.83	968	238	346	35.5	151	69.2	9.3	21.5	1.8
2011/12 and 2012/13		Natural vegetation (grass)		6.52	455	104	192	24.5	164	86.1	1.4	12.6	0.54
2011/12 and 2012/13		Natural vegetation (grass)		5.93	810	121	375	25	419	83.7	3.8	12.5	2.54
2012/13	Viljoens-kroon	Glyphosate-soybean tolerant (PAN1583R)	Maize/Soybean	6.82	381	96	330	5	295	94.1	1.2	4.7	0.2
2012/13		Natural vegetation (grass)		6.14	433	195	370	9.5	227	84.4	5.9	9.7	1.14
2011/12 and 2012/13	Winterton	Glyphosate-tolerant soybean (PAN6164R)	Soybean	5.67	1,782	400.5	381	20.5	85	81.2	10.4	8.5	2.49
2012/13		Conventional soybean (Mukwa)	Maize/ Soybean	6.33	1,565	198	182	2	390	78.8	12.9	8.4	1.3
2011/12 and 2012/13		Conventional soybean (Mukwa)	Maize/Soybean	5.92	1,827	139	551	5.5	532	44.8	38.4	16.7	2.77
2011/12 and 2012/13		Natural vegetation (grass)		6.85	751	120	86	0.5	335	61.4	23.3	15.3	1.62
2011/12 and 2012/13		Natural vegetation (grass)		5.65	887	208	295	4.5	358	45.9	31.4	22.8	2.59

Average temperature and rainfall figures for the 28 sites where a nematode survey was conducted during the 2011/12 and 2012/13 growing seasons_

		Temperature (°C)
Locality and province	Growing season	Min.	Max.	Rainfall (mm)
Bothaville (Free State)	2011/12	13	26	272
	2012/13	14	30	255
Brits (North West)	2011/12	16	33	414
	2012/13	16	32	365
Edenville (Free State)	2012/13	16	32	303
Marble Hall (Mpumalanga)	2011/12	18	31	402
	2012/13	18	35	353
Viljoenskroon (Free State)	2012/13	14	31	373
Winterton (Kwa-Zulu Natal)	2011/12	14	30	409
	2012/13	14	30	417

Non-parasitic nematodes associated with soybean and natural vegetation at 28 sites in the soybean production areas of South Africa during the 2011/12 and 2012/13 growing seasons (√ indicates the presence of a genus; – indicates the absence of a genus)_

Genus	Functional guild^a, followed by c–p value^b	Glyphosate-tolerant soybean	Conventional soybean	Natural vegetation
Mesorhabditis (Osche, 1952; Dougherty, 1953)	Ba1	√	√	√
Panagrolaimus (Fuchs, 1930)	Ba1	√	√	√
Rhabditis (Dujardin, 1845)	Ba1	√	√	√
Acrobeles (Linstow, 1877)	Ba2	√	√	√
Acrobeloides (Cobb, 1924; Thorne, 1937)	Ba2	√	√	√
Cephalobus (Steiner, 1929)	Ba2	√	√	√
Chiloplacus (Thorne, 1937)	Ba2	√	√	√
Eucephalobus (Steiner, 1936)	Ba2	√	√	√
Monhystera (Bastian, 1865)	Ba2	√	√	√
Plectus (Bastian, 1865)	Ba2	√	√	√
Seleborca (Andrassy, 1985)	Ba2	√	√	√
Wilsonema (Cobb, 1913)	Ba2	√	√	√
Zeldia (Thorne, 1937)	Ba2	√	√	√
Teratocephalus (de Man, 1876)	Ba4	√	√	√
Alaimus (de Man, 1880)	Ba4	√	√	√
Aphelenchoides (Fischer, 1894)	Fu2	√	√	√
Aphelenchus (Bastian, 1865; Cobb, 1927)	Fu2	√	√	√
Ditylenchus (Filipjev, 1936)	Fu2	√	√	√
Psilenchus (de Man, 1921)	Fu2	√	√	√
Tylenchus (Bastian, 1865)	Fu2	√	√	√
Coslenchus (Siddiqi, 1978)	Fu3	√	√	√
Leptonchus (Cobb, 1920)	Fu4	√	√	√
Tylencholaimellus (Cobb, 1915; de Man, 1921)	Fu4	√	√	√
Tylencholaimus (de Man, 1880)	Fu4	√	√	√
Dorylaimus (Thorne, 1939)	Om4	√	√	√
Eudorylaimus (Andrassy, 1959)	Om4	√	√	√
Thornenema (Andrassy, 1959)	Om4	√	√	√
Mononchus (Chitwood and Allen, 1959)	Pr4	√	√	√
Paraxonchium (Krall, 1958)	Pr4	√	√	√
Aporcelaimellus (Heyns, 1965)	Pr5	√	√	√
Discolaimium (Thorne, 1939)	Pr5	√	√	√
Discolaimoides (Heyns, 1963)	Pr5	√	√	√

Terrestrial Non-Parasitic Nematode Assemblages associated With Glyphosate-tolerant and Conventional Soybean-Based Cropping Systems

Figures & Tables

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Crop history, agricultural practices, fertilisers applied, glyphosate application dates, and dosage rate, nematode sampling dates, rainfall, and minimum and maximum temperatures recorded of the experimental plot during the 2013/14 and 2014/15 growing seasons_

Soybean cultivar planted at each soybean field, crop history, and selected soil chemical and physical properties of each field where plant-parasitic nematodes from roots and rhizosphere soil samples were collected during the 2011/12 and 2012/13 growing seasons_

Average temperature and rainfall figures for the 28 sites where a nematode survey was conducted during the 2011/12 and 2012/13 growing seasons_

Non-parasitic nematodes associated with soybean and natural vegetation at 28 sites in the soybean production areas of South Africa during the 2011/12 and 2012/13 growing seasons (√ indicates the presence of a genus; – indicates the absence of a genus)_

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