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

Akhona Mbatyoti
Akhona Mbatyoti
, 
Mieke Stefanie Daneel
Mieke Stefanie Daneel
, 
Antoinette Swart
Antoinette Swart
, 
Dirk de Waele
Dirk de Waele
 oraz 
Hendrika Fourie
Hendrika Fourie
   | 17 paź 2018
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Data publikacji: 17 paź 2018
Zakres stron: 243 - 260
DOI: https://doi.org/10.21307/jofnem-2018-028
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© 2018 Akhona Mbatyoti et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

Fig. 1

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).
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).

Fig. 2

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.
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.

Fig. 3

(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.
(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).
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
Season*Ecosystem*Locality 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 guilda, followed by c–p valueb 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 √ √ √
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