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

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

Journal of Nematology
Volume 53 (2021): Issue 1 (January 2021)
By: Raquel Campos-Herrera,  Ignacio Vicente-Díez,  Magda Galeano,  Maryam Chelkha,  María del Mar González-Trujillo,  Miguel Puelles,  David Labarga,  Alicia Pou,  Javier Calvo and  José Eduardo Belda  
Open Access
|Dec 2021

Figures & Tables

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 speciesPopulationOriginITS sequence (GenBank accession number)
S. feltiae RS-5SwitzerlandKJ938569
AM-25PortugalMG551674
RM-107SpainMW480131
KoppertCommercial-
S. carpocapsae MG-596aSwitzerlandMZ914694
KoppertCommercial-
H. bacteriophora MG-618bSwitzerlandMZ914695
AM-203PortugalMG551676
RM-102SpainMW480132
KoppertCommercial-

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 speciesVariableEPN species or populationsConcentration (C)Population (P)Interaction C*P
F. occidentalis % Adult emercenceHb 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 emercenceHb 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 mortalityHb 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 killHb 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 speciesVariableEPN populations500 IJs250 IJs (F. occidentalis) 100 IJs (T. absoluta)
F. occidentalis % Adult emercenceHb 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 emercenceHb 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 mortalityHb 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 killHb 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 populationsInsectsVariableComparative 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 = 0.289No 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
DOI: https://doi.org/10.21307/jofnem-2021-102 | Journal eISSN: 2640-396X | Journal ISSN: 0022-300X
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Language: English
Page range: 1 - 14
Submitted on: Sep 14, 2021
Published on: Dec 14, 2021
Published by: Society of Nematologists, Inc.
In partnership with: Paradigm Publishing Services
Publication frequency: 1 issue per year
Keywords:
Tomato,
Aerial insect-pests
Related subjects:
Life sciences,
Life sciences, other

© 2021 Raquel Campos-Herrera, Ignacio Vicente-Díez, Magda Galeano, Maryam Chelkha, María del Mar González-Trujillo, Miguel Puelles, David Labarga, Alicia Pou, Javier Calvo, José Eduardo Belda, published by Society of Nematologists, Inc.
This work is licensed under the Creative Commons Attribution 4.0 License.

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