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Intraspecific virulence of entomopathogenic nematodes against the pests Frankliniella occidentalis (Thysanoptera: Thripidae) and Tuta absoluta (Lepidoptera: Gelechiidae)

Raquel Campos-Herrera
Raquel Campos-Herrera
, 
Ignacio Vicente-Díez
Ignacio Vicente-Díez
, 
Magda Galeano
Magda Galeano
, 
Maryam Chelkha
Maryam Chelkha
, 
María del Mar González-Trujillo
María del Mar González-Trujillo
, 
Miguel Puelles
Miguel Puelles
, 
David Labarga
David Labarga
, 
Alicia Pou
Alicia Pou
, 
Javier Calvo
Javier Calvo
 y 
José Eduardo Belda
José Eduardo Belda
   | 14 dic 2021
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Publicado en línea: 14 dic 2021
Páginas: 1 - 14
Recibido: 14 sept 2021
DOI: https://doi.org/10.21307/jofnem-2021-102
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© 2021 Raquel Campos-Herrera et al., published by Sciendo.
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Figure 1:

Intraspecific virulence of various populations from three entomopathogenic nematodes (EPN) species (Steinernema feltiae, Steinernema carpocapase, and Heterorhabditis bacteriophora) against Frankliniella occidentalis. (A) Percentage of F. occidentalis adult emergence after the application of four H. bacteriophora populations. (B) Percentage of F. occidentalis adult emergence after the application of four S. feltiae populations. (C) Percentage of F. occidentalis adult emergence after the application of two S. carpocapsae populations. Each population was applied in two concentrations: 500 JIs (160/cm2) and 250 JIs (80 IJs/cm2). Different small letters indicate significant differences in Tukey’s test (HSD) for the low concentration analysis. Different capital letters indicate significant differences in Tukey’s test (HSD). Above each species, asterisks indicate significant differences within treatment t student comparisons at *P < 0.05, **P < 0.01, ***P < 0.001, and n.s., not significant. Values are least-square means ± SE.
Intraspecific virulence of various populations from three entomopathogenic nematodes (EPN) species (Steinernema feltiae, Steinernema carpocapase, and Heterorhabditis bacteriophora) against Frankliniella occidentalis. (A) Percentage of F. occidentalis adult emergence after the application of four H. bacteriophora populations. (B) Percentage of F. occidentalis adult emergence after the application of four S. feltiae populations. (C) Percentage of F. occidentalis adult emergence after the application of two S. carpocapsae populations. Each population was applied in two concentrations: 500 JIs (160/cm2) and 250 JIs (80 IJs/cm2). Different small letters indicate significant differences in Tukey’s test (HSD) for the low concentration analysis. Different capital letters indicate significant differences in Tukey’s test (HSD). Above each species, asterisks indicate significant differences within treatment t student comparisons at *P < 0.05, **P < 0.01, ***P < 0.001, and n.s., not significant. Values are least-square means ± SE.

Figure 2:

Intraspecific virulence of various populations from three entomopathogenic nematodes (EPN) species (Steinernema feltiae, Steinernema carpocapase, and Heterorhabditis bacteriophora) against pupa of Tuta absoluta. (A) Percentage of T. absoluta adult emergence after the application of four H. bacteriophora populations. (B) Percentage of F. occidentalis adult emergence after the application of four S. feltiae populations. (C) Percentage of F. occidentalis adult emergence after the application of two S. carpocapsae populations. Each population was applied in two concentrations: 500 JIs (21/cm2) and 100 JIs (4 IJs/cm2). Different small letters indicate significant differences in Tukey’s test (HSD) for the low concentration analysis. Different capital letters indicate significant differences in Tukey’s test (HSD). Above each species, asterisks indicate significant differences within treatment t student comparisons at *P < 0.05, **P < 0.01, ***P < 0.001, and n.s., not significant. Values are least-square means ± SE.
Intraspecific virulence of various populations from three entomopathogenic nematodes (EPN) species (Steinernema feltiae, Steinernema carpocapase, and Heterorhabditis bacteriophora) against pupa of Tuta absoluta. (A) Percentage of T. absoluta adult emergence after the application of four H. bacteriophora populations. (B) Percentage of F. occidentalis adult emergence after the application of four S. feltiae populations. (C) Percentage of F. occidentalis adult emergence after the application of two S. carpocapsae populations. Each population was applied in two concentrations: 500 JIs (21/cm2) and 100 JIs (4 IJs/cm2). Different small letters indicate significant differences in Tukey’s test (HSD) for the low concentration analysis. Different capital letters indicate significant differences in Tukey’s test (HSD). Above each species, asterisks indicate significant differences within treatment t student comparisons at *P < 0.05, **P < 0.01, ***P < 0.001, and n.s., not significant. Values are least-square means ± SE.

Figure 3:

Intraspecific virulence of various populations from three entomopathogenic nematodes (EPN) species (Steinernema feltiae, Steinernema carpocapase, and Heterorhabditis bacteriophora) against last instar Tuta absolua. (A) Percentage of T. absoluta larval mortality after the application of four H. bacteriophora populations. (B) Percentage of T. absoluta larval mortality after the application of four S. feltiae populations. (C) Percentage of T. absoluta larval mortality after the application of two S. carpocapsae populations. Each population was applied in two concentrations: 500 JIs (21/cm2) and 100 JIs (4 IJs/cm2). Different small letters indicate significant differences in Tukey’s test (HSD) for the low concentration analysis. Different capital letters indicate significant differences in Tukey’s test (HSD). Above each species, asterisks indicate significant differences within treatment t student comparisons at *P < 0.05, **P < 0.01, ***P < 0.001, and n.s., not significant. Values are least-square means ± SE.
Intraspecific virulence of various populations from three entomopathogenic nematodes (EPN) species (Steinernema feltiae, Steinernema carpocapase, and Heterorhabditis bacteriophora) against last instar Tuta absolua. (A) Percentage of T. absoluta larval mortality after the application of four H. bacteriophora populations. (B) Percentage of T. absoluta larval mortality after the application of four S. feltiae populations. (C) Percentage of T. absoluta larval mortality after the application of two S. carpocapsae populations. Each population was applied in two concentrations: 500 JIs (21/cm2) and 100 JIs (4 IJs/cm2). Different small letters indicate significant differences in Tukey’s test (HSD) for the low concentration analysis. Different capital letters indicate significant differences in Tukey’s test (HSD). Above each species, asterisks indicate significant differences within treatment t student comparisons at *P < 0.05, **P < 0.01, ***P < 0.001, and n.s., not significant. Values are least-square means ± SE.

Figure S1:

Intraspecific virulence of various populations from three entomopathogenic nematodes (EPN) species (Steinernema feltiae, Steinernema carpocapase, and Heterorhabditis bacteriophora) against last instar Tuta absolua. A. Number of days to kill T. absoluta larvae after the application of four H. bacteriophora populations. B. Number of days to kill T. absoluta larvae after the application of four S. feltiae populations. C. Number of days to kill T. absoluta larvae after the application of two S. carpocapsae populations. Each population was applied in two concentrations: 500 JIs (21/cm 2 ) and 100 JIs (4 IJs/cm 2 ). Different small letters indicate significant differences in Tukey’s test (HSD) for the low concentration analysis. Different capital letters indicate significant differences in Tukey’s test (HSD). Above each species, asterisks indicate significant differences within treatment t student comparisons at *P < 0.05, **P < 0.01, ***P < 0.001, and n.s., not significant. Values are least-square means ± SE.
Intraspecific virulence of various populations from three entomopathogenic nematodes (EPN) species (Steinernema feltiae, Steinernema carpocapase, and Heterorhabditis bacteriophora) against last instar Tuta absolua. A. Number of days to kill T. absoluta larvae after the application of four H. bacteriophora populations. B. Number of days to kill T. absoluta larvae after the application of four S. feltiae populations. C. Number of days to kill T. absoluta larvae after the application of two S. carpocapsae populations. Each population was applied in two concentrations: 500 JIs (21/cm 2 ) and 100 JIs (4 IJs/cm 2 ). Different small letters indicate significant differences in Tukey’s test (HSD) for the low concentration analysis. Different capital letters indicate significant differences in Tukey’s test (HSD). Above each species, asterisks indicate significant differences within treatment t student comparisons at *P < 0.05, **P < 0.01, ***P < 0.001, and n.s., not significant. Values are least-square means ± SE.

Populations and species of nematodes of the genera Steinernema and Heterorhabditis investigated in this study

Entomopathogenic nematode species Population Origin ITS sequence (GenBank accession number)
S. feltiae RS-5 Switzerland KJ938569
AM-25 Portugal MG551674
RM-107 Spain MW480131
Koppert Commercial -
S. carpocapsae MG-596a Switzerland MZ914694
Koppert Commercial -
H. bacteriophora MG-618b Switzerland MZ914695
AM-203 Portugal MG551676
RM-102 Spain MW480132
Koppert Commercial -

Statistical analysis of the effect of two factors (infective juvenile concentration and EPN population) and their interactions (GLM, P < 0.05) for the variables percentage of adult emercence for Frankliniella occidentalis and Tuta absoluta, and the larval mortality percentage and number of days to kill the last instar larvae of T. absoluta. Analysis performed considering each of the popualtions of the three species Heterorhabditis bacteriophora (Hb), Steinernema feltiae (Sf), and S. carpocapsae (Sc).

Insect species Variable EPN species or populations Concentration (C) Population (P) Interaction C*P
F. occidentalis % Adult emercence Hb populations F  = 5.474, P  = 0.020 F  = 8.357, P  < 0.001 F  = 4.757, P  = 0.001
Sf populations F  = 1.564, P = 0.211 F  = 15.374, P  < 0.001 F = 1.533, P = 0.190
Sc populations F  = 6.951, P  = 0.009 F  = 11.103, P  < 0.001 F  = 4.636, P  = 0.010
T. absoluta % Adult emercence Hb populations F  = 9.885, P  = 0.002 F  = 15.925, P  < 0.001 F  = 4.067, P  = 0.003
Sf populations F = 0.963, P = 0.327 F = 7.794, P  < 0.001 F = 0.496, P = 0.739
Sc populations F  = 10.655, P  = 0.001 F  = 7.080, P  = 0.001 F = 2.178, P = 0.114
% Larval mortality Hb populations F  = 14.531, P  < 0.001 F  = 90.407, P  < 0.001 F = 1.468, P = 0.210
Sf populations F  = 7.649, P  = 0.006 F  = 1609.766, P  < 0.001 F = 1.278, P = 0.277
Sc populations F  = 18.917, P  < 0.001 F  = 340.796, P  < 0.001 F = 2.989, P = 0.051
No. Days to kill Hb populations F  = 9.455, P  = 0.002 F  = 4.973, P  = 0.001 F  = 3.367, P  = 0.010
Sf populations F  = 1.686, P = 0.195 F  = 39.515, P  < 0.001 F  = 11.649, P  < 0.001
Sc populations F  = 5.179, P  = 0.023 F  = 11.109, P  < 0.001 F  = 7.471, P  = 0.001

Statistical analysis of the effect of infective juvenile (IJs) concentration (ANOVA, P < 0.05) for the variables percentage of adult emercence for Frankliniella occidentalis and Tuta absoluta, and the larval mortality percentage and number of days to kill the last instar larvae of T. absoluta. Analysis performed considering the popualtions of each the three species Heterorhabditis bacteriophora (Hb), Steinernema feltiae (Sf), and S. carpocapsae (Sc).

Insect species Variable EPN populations 500 IJs 250 IJs (F. occidentalis) 100 IJs (T. absoluta)
F. occidentalis % Adult emercence Hb populations F 4,499  = 10.192, P  < 0.001 F 4,489  = 3.006, P  = 0.018
Sf populations F 4,550  = 11.148, P  < 0.001 F 4,549  = 5.714, P  < 0.001
Sc populations F 2,292  = 6.766, P  = 0.001 F 2,303  = 8.734, P  < 0.001
T. absoluta % Adult emercence Hb populations F 4,398  = 19.722, P  < 0.001 F 4,398 = 2.007, P = 0.093
Sf populations F 4,398  = 4.140, P  = 0.003 F 4,399  = 4.149, P  = 0.003
Sc populations F 2,239  = 17.490, P  < 0.001 F 2,239 = 0.465, P = 0.629
% Larval mortality Hb populations F 4,443  = 64.645, P  < 0.001 F 4,439  = 33.101, P  < 0.001
Sf populations F 4,473  = 1001.35, P  < 0.001 F 4,439  = 681.218, P  < 0.001
Sc populations F 2,271  = 243.946, P  < 0.001 F 2,278  = 133.477, P  < 0.001
No. Days to kill Hb populations F 4,327  = 3.169, P  = 0.014 F 4,476  = 4.737, P  < 0.001
Sf populations F 4,388  = 40.353, P  < 0.001 F 4,378  = 22.344, P  < 0.001
Sc populations F 2,473 = 0.917, P = 0.401 F 2,178  = 13.606, P  < 0.001

Statistical analysis of the effect of the entomopathogenic nematodes (EPNs) infective juvenile (IJs) concentration (ANOVA, P < 0.05) for the variables percentage of adult emercence for Frankliniella occidentalis and Tuta absoluta, and the larval mortality percentage and number of days to kill the last instar larvae of T. absoluta. Analysis performed considering the control (C), and each of the populations of the three species Heterorhabditis bacteriophora (Hb), Steinernema feltiae (Sf), and S. carpocapsae (Sc).

EPNs or populations Insects Variable Comparative between concentrations
H. bacteriophora C Koppert RM-102 AM-203 MG-618b
F. occidentalis % Adult emercence t 188  = 2.475, P  = 0.016 t 198 = 0.153, P = 0.879 t 198  = 3.545, P  = 0.001 t 198 = 1.929, P = 0.055 t 198 = 1.845, P = 0.067
T. absoluta % Adult emercence t 158 = 1.856, P = 0.065 t 158 = 1.105, P = 0.271 t 158 = 1.426, P = 0.156 t 157  = 3.398, P  = 0.001 t 157  = 3.117, P  = 0.002
% Larval mortality t 182 = 0.046, P = 0.963 t 174  = 2.383, P  = 0.018 t 174  = 2.766, P  = 0.006 t 174 = 1.465, P = 0.145 t 174 = 1.898, P = 0.060
No. Days to kill t 38 = 0.103, P = 0.919 t 111  = 3.198, P  = 0.002 t 139  = 3.406, P  = 0.002 t 150 = 1.431, P = 0.155 t 159 = 0.272, P = 0.786
S. feltiae C Koppert RM-107 RS-5 AM-25
F. occidentalis % Adult emercence t 299 = 0.028, P = 0.979 t 198  = 2.288, P  = 0.023 t 198 = 0.880, P = 0.380 t 198 = 0.721, P = 0.472 t 198 = 0.423, P = 0.673
T. absoluta % Adult emercence t 158 = 0.532, P = 0.595 t 158 = 0.157, P = 0.875 t 157 = 0.566, P = 0.572 t 158 = 0.476, P = 0.635 t 158 = 1.432, P = 0.154
% Larval mortality t 185 = 1.211, P = 0.289 No calcule* P = 1.0 t 190  = 2.032, P  = 0.045 t 188  = 2.011, P  = 0.045 No calcule* P = 1.0
No. days to kill t 10 = 2.066, P = 0.066 t 189 = 0.570, P = 0.569 t 186  = 4.723, P  < 0.001 t 184  = 2.882, P  = 0.004 t 189  = 2.043, P  = 0.045
S. carpocapsae C Koppert MG-596a
F. occidentalis % Adult emercence t 216 = 0.804, P = 0.422 t 177  = 3.692, P  < 0.001 t 198 = 1.601, P = 0.111
T. absoluta % Adult emercence t 158 = 0.532, P = 0.595 t 158  = 2.313, P  = 0.022 t 158  = 2.761, P  = 0.006
% Larval mortality t 165 = 1.445, P = 0.153 t 190  = 2.285, P  = 0.025 t 190  = 4.241, P  < 0.001
No. Days to kill t 30 = 0.210, P = 0.835 t 186 = 0.169, P = 0.866 t 166  = 4.884, P  < 0.001
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