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The Efficacy of Entomopathogenic Nematodes Plus an Adjuvant against Helicoverpa zea and Chrysodeixis includens in Aboveground Applications

Minling Zhang
Minling Zhang
, 
Nathan Spaulding
Nathan Spaulding
, 
Gadi V.P. Reddy
Gadi V.P. Reddy
 and 
David I Shapiro-Ilan
David I Shapiro-Ilan
   | May 08, 2024
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Article Category: Research Paper
Published Online: May 08, 2024
Page range: -
Received: Jan 17, 2024
DOI: https://doi.org/10.2478/jofnem-2024-0018
Keywords
© 2024 Minling Zhang, published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

Figure 1:

EPN infection on eggs of Helicoverpa zea and Chrysodeixis includens. (A) An infectious juvenile of Steinernema carpocapsae (all strain) was infecting an egg of H. zea with part of its body inside the egg. (B) An infected egg of H. zea by Heterorhabditis georgiana (kesha strain), from which 50 progeny juveniles were produced. (C) A larva of H. zea killed inside an egg by H. floridensis (K22) with young juveniles inside four adult female nematodes. (D) A larva of C. includens killed inside an egg by a juvenile of S. feltiae (SN). (E) A head capsule of a C. includens larva left after a juvenile of S. feltiae (SN) developed inside the egg. (F) A head capsule of a C. includens larva inside an egg with newly emerged juveniles of S. feltiae (SN).
EPN infection on eggs of Helicoverpa zea and Chrysodeixis includens. (A) An infectious juvenile of Steinernema carpocapsae (all strain) was infecting an egg of H. zea with part of its body inside the egg. (B) An infected egg of H. zea by Heterorhabditis georgiana (kesha strain), from which 50 progeny juveniles were produced. (C) A larva of H. zea killed inside an egg by H. floridensis (K22) with young juveniles inside four adult female nematodes. (D) A larva of C. includens killed inside an egg by a juvenile of S. feltiae (SN). (E) A head capsule of a C. includens larva left after a juvenile of S. feltiae (SN) developed inside the egg. (F) A head capsule of a C. includens larva inside an egg with newly emerged juveniles of S. feltiae (SN).

Figure 2:

Larvae of (A) Helicoverpa zea and (B) Chrysodeixis includens inside eggs where larvae biting the eggshells and the protruding hairs of larvae were visible. (C) An adult of Heterorhabditis floridensis (K22 strain) from an H. zea egg with a few juveniles inside its body, and (D) two adults of Steinernema carpocapsae (all strain) from a fifth instar of C. includens with many juveniles inside one adult and eggs inside another.
Larvae of (A) Helicoverpa zea and (B) Chrysodeixis includens inside eggs where larvae biting the eggshells and the protruding hairs of larvae were visible. (C) An adult of Heterorhabditis floridensis (K22 strain) from an H. zea egg with a few juveniles inside its body, and (D) two adults of Steinernema carpocapsae (all strain) from a fifth instar of C. includens with many juveniles inside one adult and eggs inside another.

Figure 3:

EPN infection of larvae and pupae of Helicoverpa zea and Chrysodeixis includens. (A) Adults of Steinernema rarum (17c+e strain) inside a larva of H. zea. (B) Large adults of S. carpocapsae (all) inside the head of C. includens larva. (C) Juveniles of S. riobrave (7–12) from a pupa of H. zea in a White trap. (D) Adults of Heterorhabditis georgiana (kesha strain) inside a pupa of Chrysodeixis includens.
EPN infection of larvae and pupae of Helicoverpa zea and Chrysodeixis includens. (A) Adults of Steinernema rarum (17c+e strain) inside a larva of H. zea. (B) Large adults of S. carpocapsae (all) inside the head of C. includens larva. (C) Juveniles of S. riobrave (7–12) from a pupa of H. zea in a White trap. (D) Adults of Heterorhabditis georgiana (kesha strain) inside a pupa of Chrysodeixis includens.

Figure 4:

EPN suspension with and without an adjuvant. (A) Without an adjuvant, suspension was distributed unevenly on a corn leaf; air bubbles were visible. (B) With SAg Surfactant, suspension was distributed evenly across the corn leaf, which may help nematodes to find hosts and hide in pores on a corn leaf. (C) Without an adjuvant, many EPNs were trapped in water droplets, including on the leaf and insect. (D) With SAg Surfactant, a juvenile was able to search and move around more freely, allowing it to attempt to hide in a small leaf gap when the leaf was getting dry.
EPN suspension with and without an adjuvant. (A) Without an adjuvant, suspension was distributed unevenly on a corn leaf; air bubbles were visible. (B) With SAg Surfactant, suspension was distributed evenly across the corn leaf, which may help nematodes to find hosts and hide in pores on a corn leaf. (C) Without an adjuvant, many EPNs were trapped in water droplets, including on the leaf and insect. (D) With SAg Surfactant, a juvenile was able to search and move around more freely, allowing it to attempt to hide in a small leaf gap when the leaf was getting dry.

Effect of Steinernema carpocapsae (all strain) with an adjuvant on first instars of Helicoverpa zea in corn plants in a corn field (2022, Leland, Mississippi).

Field exp., # Experiment date Temperature RH Weather condition EPN Rate Plant Age Plant high Treatment # of Insects % Mortality ± SEM % EPN Infection ± SEM
Field exp, #1 20 IJs/cm2 S. carpocapsae (All) + SAg^ 63 78.2 ± 9.2 a 35.0 ± 10.3 a
June 17, 2022
24(23–35) °Ca 6 wk S. carpocapsae (All) 56 69.3 ± 7.8 a 24.2 ± 10.2 a
82(62–99) %RH 1.1 m Water + SAg 64 22.0 ± 4.6 b 0.0 ± 0.0 b
30 min heavy rain Water 53 28.0 ± 8.1 b 0.0 ± 0.0 b
F(3, 12)=20.66 F(3, 12)=10.95
P < 0.0001 P < 0.0009
Field exp., #2 40 IJs/cm2 S. carpocapsae (All) + SAg 80 87.7 ± 1.1 a 66.4 ± 4.7 a
June 27, 2022
22(19–30) °C 7.5 wk S. carpocapsae (All) 58 70.4 ± 3.6 b 42.0 ± 2.5 b
83(58–94) %RH 1.3 m Water + SAg 65 18.7 ± 4.5 c 0.0 ± 0.0 c
Partly Cloudy Water 74 21.6 ± 3.1 c 0.0 ± 0.0 c
F(3, 12)=77.26 F(3, 12)=294.09
P < 0.0001 P < 0.0001)

Effect of Steinernema riobrave (7–12 strain) and Steinernema carpocapsae (all strain) with an adjuvant on fifth instars of Chrysodeixis includens on soybean plants in soybean fields (2022, Leland, Mississippi).

Experiment date Temperature RH Weather condition EPN rate Plant age Plant high Treatment # of Insects % Mortality ± SEM % EPN Infection ± SEM
Field exp., #1 August 3, 2022 40 IJs/cm2 S. carpocapsae (All) + SAg^ 37 92.9 ± 4.7 a 37.1 ± 7.6 a
24(22–35) °Ca 9 wk S. riobrave (7–12) + SAg 51 25.2 ± 12.6 b 0.0 ± 0.0 b
88(60–97) %RH 0.5 m Water + SAg 38 13.0 ± 7.2 b 0.0 ± 0.0 b
Most sunny F(2, 9)=16.82 F(2, 9)=58.4
P=0.0009 P < 0.0001
Field exp., #2 September 8, 2022 10 IJs/cm2 S. carpocapsae (All) + SAg 95 23.7 ± 4.8 a 7.1 ± 1.4 a
22(19–32) °C 8 wk S. riobrave (7–12) + SAg 91 6.2 ± 1.3 b 0.0 ± 0.0 b
79(40–95) %RH 0.4 m Water + SAg 84 1.09 ± 1.1 b 0.0 ± 0.0 b
Sunny F(2, 9)=21.28 F(2, 9)=73.04
P=0.0004 P < 0.0001

Entomopathogenic nematodes infection (% ± SEM)) on eggs of Helicoverpa zea and Chrysodeixis includens in the laboratory (25°C, 85% RH).

EPN strain H. zea C. includens
Unfertilized eggsa Mixed eggs Mixed eggs
Heterorhabditis bacteriophora (HP88) 0.0 ± 0.0 a 5.0 ± 3.4 ab 6.7 ± 3.3 a
Heterorhabditis bacteriophora (VS) 1.7 ± 1.7 a 1.7 ± 1.7 ab 0.0 ± 0.0 a
Heterorhabditis floridensis (K22) 6.7 ± 3.3 a 10.0 ± 6.3 ab 0.0 ± 0.0 a
Heterorhabditis georgiana (kesha) 0.0 ± 0.0 a 11.7 ± 4.0 a 0.0 ± 0.0 a
Steinernema carpocapsae (All) 1.7 ± 1.7 a 0.0 ± 0.0 b 1.7 ± 1.7 a
Steinernema carpocapsae (Cxrd) 1.7 ± 1.7 a 3.3 ± 1.7 ab 1.7 ± 1.7 a
Steinernema feltiae (SN) 0.0 ± 0.0 a 3.3 ± 2.1 ab 6.7 ± 4.9 a
Steinernema rarum (17c+e) 0.0 ± 0.0 a 1.7 ± 1.7 ab 0.0 ± 0.0 a
Steinernema riobrave (355) 1.7 ± 1.7 a 6.7 ± 2.1 ab 0.0 ± 0.0 a
Steinernema riobrave (7–12) 1.7 ± 1.7 a 0.0 ± 0.0 b 3.3 ± 3.3 a
Water 0.0 ± 0.0 a 0.0 ± 0.0 b 0.0 ± 0.0 a
F-value (10, 55) 1.53 2.64 1.64
P-value 0.1534 0.0104 0.1193

Mortality (% ± SEM) of first to fourth instars, fifth instars, and pupae of Helicoverpa. zea and Chrysodeixis includens caused by 10 entomopathogenic nematode strains in the laboratory (25°C, 85% RH).

EPN strains H. zea C. includens H. zea and C. includens
First-fourth instars Fifth instars Pupae First-fourth instars Fifth instars Pupae Avg of first-fourthand fifth instarsa
Heterorhabditis bacteriophora (HP88) 100.0 ± 0.0 a 81.7 ± 6.0 ab 6.7 ± 4.9 ab 80.0 ± 7.3 a 96.7 ± 2.1 a 33.3 ± 11.7 abc 89.6
Heterorhabditis bacteriophora (VS) 98.3 ± 1.7 a 81.7 ± 4.8 ab 15.0 ± 4.3 ab 72.6 ± 5.4 ab 93.3 ± 4.9 a 40.0 ± 11.8 ab 86.5
Heterorhabditis floridensis (K22) 98.3 ± 1.7 a 85.0 ± 7.6 ab 21.7 ± 8.7 ab 88.3 ± 3.1 a 100.0 ± 0.0 a 30.0 ± 8.9 abc 92.9 (top 5)
Heterorhabditis georgiana (kesha) 100.0 ± 0.0 a 83.3 ± 4.2 ab 13.3 ± 4.2 ab 90.0 ± 4.5 a 95.0 ± 3.4 a 45.0 ± 5.0 ab 92.0 (top 5)
Steinernema carpocapsae (All) 100.0 ± 0.0 a 95.0 ± 3.4 a 20.0 ± 6.8 ab 85.0 ± 2.2 a 98.3 ± 1.7 a 41.7 ± 9.5 ab 94.6 (top 5)
Steinernema carpocapsae (Cxrd) 100.0 ± 0.0 a 85.0 ± 8.1 ab 21.7 ± 6.0 ab 80.0 ± 8.6 a 98.3 ± 1.7 a 36.7 ± 12.3 ab 90.8
Steinernema feltiae (SN) 100.0 ± 0.0 a 76.7 ± 6.7 ab 5.0 ± 2.2 ab 40.0 ± 5.8 b 95.0 ± 3.4 a 18.3 ± 6.0 bc 77.9
Steinernema rarum (17c+e) 100.0 ± 0.0 a 58.3 ± 13.8 b 13.3 ± 5.6 ab 71.7 ± 7.4 ab 88.3 ± 7.9 a 26.7 ± 4.9 abc 79.6
Steinernema riobrave (355) 100.0 ± 0.0 a 88.3 ± 5.4 ab 21.7 ± 6.5 a 86.7 ± 6.1 a 100.0 ± 0.0 a 61.7 ± 7.0 a 93.8 (top 5)
Steinernema riobrave (7–12) 100.0 ± 0.0 a 93.3 ± 4.9 a 15.0 ± 4.3 ab 90.0 ± 5.2 a 98.3 ± 1.7 a 63. 3 ± 4.2 a 95.4 (top 5)
Water 3.3 ± 3.3 b 0.0 ± 0.0 c 0.0 ± 0.0 b 0.0 ± 0.0 c 0.0 ± 0.0 b 1.7 ± 1.7 c 0
F-Value (10, 55) 187.99 15.81 2.42 18.4 41.62 4.99
P-Value <.0001 <.0001 0.0184 <.0001 <.0001 <.0001
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