Identification and life history of aphids associated with chili pepper crops in southwestern Colombia
Published
Jun 12, 2020
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Maria R. Manzano
https://orcid.org/0000-0002-0858-2426
William Tálaga-Taquinas
https://orcid.org/0000-0001-9845-9669
Clara Inés Melo-Cerón
https://orcid.org/0000-0002-6580-5390
Yorley Beatriz Lagos-Álvarez
https://orcid.org/0000-0001-9365-9055
Diana N. Duque-Gamboa
https://orcid.org/0000-0003-1859-8381
Nelson Toro-Perea
https://orcid.org/0000-0002-2835-7285
https://orcid.org/0000-0002-0858-2426
William Tálaga-Taquinas
https://orcid.org/0000-0001-9845-9669
Clara Inés Melo-Cerón
https://orcid.org/0000-0002-6580-5390
Yorley Beatriz Lagos-Álvarez
https://orcid.org/0000-0001-9365-9055
Diana N. Duque-Gamboa
https://orcid.org/0000-0003-1859-8381
Nelson Toro-Perea
https://orcid.org/0000-0002-2835-7285
##plugins.themes.bootstrap3.article.details##
Abstract
Viral diseases, transmitted by aphids, are the most limiting problems in chili pepper crops. Understanding the demographic features of these aphids, may thus assist the design of better disease control strategies in chili peppers. Aphid species found in chili pepper crops in south western Colombia were identified as Aphis gossypii Glover and Myzus persicae (Sulzer). An array of life-history parameters of both aphid species were investigated at (25 ± 0.5) ◦C, (75 ± 1.75) % r.h., L12:D12, and LS 5-Light Storm in chili pepper crops. Both aphid populations consisted only of parthenogenetic females, showing a similar average development time—from the first nymphal instar to the post-reproductive adult—, female longevity, and daily average fertility values. The length of the reproductive period was higher for M. persicae. A. gossypii reached its adult state significantly faster than M. persicae. The intrinsic rate of population growth (rm) was lower for M.persicae (0.39) compared to A. gossypii (0.43). Results showed a potential for fast population growth in both species, which would enhance their role as virus vectors. The information acquired is essential to develop pest management initiatives for these two aphid species.
Keywords
Aphis gossypii, Barcoding, Capsicum, Myzus persicae, rm values
References
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[8]Armstrong KF, Ball SL. DNA barcodes for biosecurity: invasive species identification, Philosophical Transactions of The Royal Society B Biological Sciences, 360: 1813-1823, 2005.
doi: 10.1098/rstb.2005.1713
[9] Piffaretti J, Vanlerberghe-Masutti F, Tayeh A, Clamens AL, D’Acier AC, Jousselin E. Molecular phylogeny reveals the existence of two sibling species in the aphid pest Brachycaudus helichrysi (Hemiptera: Aphididae), Zoologica Scripta, 41: 266-280, 2012.
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[10] Miller GL, & Foottit RG. The taxonomy of crop pests: The aphids. In: Foottit R, Adler P. eds., Insect Biodiversity: Science and Society. Blackwell Publishing, Oxford. pp. 463-473, 2009.
doi: 10.1002/9781444308211.ch20
[11] Lokeshwari D, Kumar NKK, Manjunatha H. Color polymorphism does not affect species diagnosis of the melon aphid, Aphis gossypii (Hemiptera: Aphididae), Florida Entomologist, 97: 1199-1207, 2014.
doi: 10.1653/024.097.0327
[12] Simon J-C, Peccoud J. Rapid evolution of aphid pests in agricultural environments, Current Opinion in Insect Science, 26: 17-24, 2018.
doi: 10.1016/j.cois.2017.12.009
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doi: 10.1007/978-90-481-8601-3_1
[14]Hosseini-Tabesh B, Sahragard A, Karimi-Malati A. A laboratory and field condition comparison of life table parameters of Aphis gossypii Glover (Hemiptera: Aphididae), Journal of Plant Protection Research, 55: 1-7, 2015.
doi: 10.1515/jppr-2015-0001
[15] McDonald SA, Halbert SE, Tolin SA, Nault BA. Seasonal abundance and diversity of aphids (Homoptera: Aphididae) in a pepper production region in Jamaica, Environmental Entomology, 32: 499-509, 2003.
doi: 10.1603/0046-225X-32.3.499
[16] Blackman RL, Eastop VF. Aphids on the World's Crops: An Identification and Information Guide. 2nd ed. John Wiley and Sons Ltd, Chichester, UK, 2000.
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doi: 10.1017/S0007485317001298
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doi: 10.1093/molbev/mst197
[20] Hebert PDN, Cywinska A, Ball SL. Biological identifications through DNA barcodes, Proceedings of the Royal Society of London B: Biological Sciences, 270: 313-321, 2003.
doi: 10.1098/rspb.2002.2218
[21]van Velzen R, Weitschek E, Felici G, Bakker FT. DNA barcoding of recently diverged species: Relative performance of matching methods, PloS One, 7: 304-309, 2012.
doi: 10.1371/journal.pone.0030490
[22] Ratnasingham S, Hebert PDN. BOLD: The barcode of life data system, Molecular Ecology Notes, 7: 355-364, 2007.
doi: 10.1111/j.1471-8286.2007.01678.x
[23] Carey JR. Applied demography for biologists with special emphasis on insects. 1st ed. U niversity Press, Oxford, UK, 1993.
doi: 10.1016/0169-5347(94)90043-4
[24] R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2018.
[25] Özgökçe MS, ChiH, Atlıhan R, Kara H. Demography and population projection of Myzus persicae (Sulz.) (Hemiptera: Aphididae) on five pepper (Capsicum annuum L.) cultivars, Phytoparasitica, 46: 153-167, 2018.
doi: 10.1007/s12600-018-0651-0
[26] Amaral D, VenzonM, dos Santos H, Sujii ER, Schmidt JM, Harwood JD. Non-crop plant communities conserve spider populations in chili pepper agroecosystems, Biological Control, 103: 69-77, 2016.
doi: 10.1016/j.biocontrol.2016.07.007
[27] Dixon AFG, Kindlmann P, Leps J, Holman J. Why there are so few species of aphids, especially in the tropics, The American Naturalist, 129: 580-592, 1987.
doi: 10.1086/284659
[28] Duffy C, Fealy R, Fealy RM. An improved simulation model to describe the temperature-dependent population dynamics of the grain aphid, Sitobion avenae, Ecological Modelling, 354: 140-171, 2017.
doi: 10.1016/j.ecolmodel.2017.03.011
[29] Rodriguez N, Michelotto MD, Da Silva RA, Busoli AC. Nymphal development of Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae) on eggplant at different temperatures, Bragantia, 64: 257-262, 2005.
doi: 10.1590/S0006-87052005000200013
[30] Hazell S, Groutides C, Neve B, Blackburn T, Bale J. A comparison of low temperature tolerance traits between closely related aphids from the tropics, temperate zone, and Arctic, Journal of Insect Physiology, 56: 115-122, 2010.
doi: 10.1016/j.jinsphys.2009.08.020
[31] Kersting U, Satar S, Uygun N. Effect of temperature on development rate and fecundity of apterous Aphis gossypii Glover (Hom., Aphididae) reared on Gossypium hirsutum L, Journal of Applied Entomology, 123: 23-27, 1999.
doi: 10.1046/j.1439-0418.1999.00309.x
[32] da Costa JG, Pires EV, Riffel A, Birkett MA, Bleicher E, Sant’Ana AEG. Differential preference of Capsicum spp. cultivars by Aphis gossypii is conferred by variation in volatile semiochemistry, Euphytica, 177: 299-307, 2011.
doi: 10.1007/s10681-010-0250-8
[33] Özder N, Sağlam Ö. The effects of temperature for development time , fecundity and reproduction on some ornamental aphid species, Journal of Central European Agriculture, 14: 627-635, 2013.
doi: 10.5513/JCEA01/14.2.1243
[34] Razmjou J, Moharramipour S, Fathipour Y, Seyed S. Effect of cotton cultivar on performance of Aphis gossypii (Homoptera: Aphididae) in Iran, Journal of Economic Entomology, 99: 1820– 1825, 2006.
doi: 10.1093/jee/99.5.1820
[35] Madahi K, Sahragard A, Hosseini R, Baniameri V. Life history performance of Aphis gossypii (Hemiptera: Aphididae) on six different host plants under microcosm condition, Journal of Entomological Society of Iran, 38: 151-172, 2018.
doi: 10.22117/jesi.2018.121466.1216
[36] Jaquiéry J, Stoeckel S, Larose C, Nouhaud P, Rispe C, Mieuzet L, Bonhomme J, Mahéo F, Legeai F, Gauthier J-P, PrunierLeterme N, Tagu D, Simon J-C. Genetic control of contagious asexuality in the pea aphid, PLoS Genetics, 10: 1-10, 2014.
doi: 10.1371/journal.pgen.1004838
[37] Barbosa LR, Carvalho CF, Auad AM, de Souza, B, Batista EP. Tabelas de esperança de vida e fertilidade de Myzus persicae sobre pimentão em laboratório e casa de vegetação, Bragantia, Campinas, 70: 375-382, 2011.
doi: 10.1590/s0006-87052011000200018
[38] Abdel-Salam AH, Ghanim AA, Hala AKE-S, El-Heneidy AH, Mervat KE-S. Biological and life table parameters of Myzus persicae (Sulz.) (Hemiptera: Aphididae) in relation to host plants and thermal requirements, Mansoura University Journal of Agricultural Sciences, 34: 8251-8262, 2009.
[39] Brault V, Uzest M, Monsion B, Jacquot E, Blanc S. Aphids as transport devices for plant viruses, Comptes Rendus Biologies, 333(6-7): 524-538, 2010.
doi: 10.1016/j.crvi.2010.04.001
[40] Singh K, Singh, R. Effect of temperature on the life history traits of Aphis gossypii Glover (Homoptera: Aphididae) on bottle gourd, Laginaria siceraria (Molina) Standl. (Cucurbitaceae), International Journal of Life Sciences Biotechnology and Pharma Research, 4: 179-183, 2015.
[41] Satar S, Kersting U, Uygun N. Effect of temperature on population parameters of Aphis gossypii Glover and Myzus persicae (Sulzer)(Homoptera: Aphididae) on pepper, Journal for Plant Diseases and Plant Protection, 115: 69-74, 2008.
doi: 10.1007/BF03356241
[42]Yin-jun F, Fen L, Abd Allah MAH, Xiao-qin Y, Min Z, Nicolas D, Xi-wu G. The damage risk evaluation of Aphis gossypii on wheat by host shift and fitness comparison in wheat and cotton, Journal of Integrative Agriculture, 17: 631-639, 2018.
doi: 10.1016/S2095-3119(17)61784-2
[43] Denno RF, McClure MS, Ott JR. Interspecific interactions in phytophagous insects: Competition reexamined and resurrected, Annual Review of Entomology, 40: 297-331, 1995.
doi: 10.1146/annurev.en.40.010195.001501
[44] Guerrieri E, Digilio MC. Aphid-plant interactions: A review, Journal of Plant Interactions, 3: 223-232, 2008.
doi: 10.1080/17429140802567173
[45] Caballero-López B, Bommarco R, Blanco-Moreno JM, Sans FX, Pujade-Villar J, Rundlöf M, Smith HG. Aphids and their natural enemies are differently affected by habitat features at local and landscape scales, Biological Control, 63: 222-229, 2012.
doi: 10.1016/j.biocontrol.2012.03.012
[46]Cui L, Qi H, Yang D, Yuan H Rui C. Cycloxaprid : A novel cisnitromethylene neonicotinoid insecticide to control imidaclopridresistant cotton aphid (Aphis gossypii), Pesticide Biochemistry and Physiology, 132: 1-6, 2016.
doi: 10.1016/j.pestbp.2016.02.005
[47] Zhou K, Huang J, Deng X, van der Werf W, Zhang W, Lu Y, Wu K, Wu F. Effects of land use and insecticides on natural enemies of aphids in cotton: First evidence from smallholder agriculture in the North China Plain, Agriculture, Ecosystems & Environment, 183: 176-184, 2014.
doi: 10.1016/J.AGEE.2013.11.008
[48] Ali A, Desneux N, Lu Y, Wu K. Key aphid natural enemies showing positive effects on wheat yield through biocontrol services in northern China. Agriculture, Ecosystems & Environment, 266: 1-9, 2018.
doi: 10.1016/j.agee.2018.07.012
doi: 10.1016/B978-0-12-801246-8.00006-8
[2] Blackman RL, Eastop VF. Aphids on the world’s herbaceous plants and shrubs. 1st ed. John Wiley and Sons Ltd, London, UK, 2006.
[3] FAO (Food and Agriculture Organization). Online statistical database: Production. FAOSTAT, [2016-11-06]. Retrieved from http://faostat3.fao.org/download/FB/*/E
[4] Foottit RG, Maw HEL, von Dohlen CD, Hebert PDN. Species identification of aphids (Insecta: Hemiptera: Aphididae) through DNA barcodes, Molecular Ecology Resources, 8: 1189-1201, 2008.
doi: 10.1111/j.1755-0998.2008.02297.x
[5] Jalalizand AR, Mirhendi H, Karimi A, Modaresi M, Mahmoodi E. Morphological and molecular identification aphids of rosae, APCBEE Procedia, 4: 12-15, 2012
doi: 10.1016/j.apcbee.2012.11.003
[6] Tsuchida T. Molecular basis and ecological relevance of aphid body colors, Current Opinion in Insect Science, 17: 74-80, 2016.
doi: 10.1016/j.cois.2016.07.005
[7]Blackman RL, Eastop VF. Taxonomic Issues. In: van Emden H. F.& Harrington R., eds. Aphids as Crop Pests. CABI, London, pp. 1-29, 2007.
[8]Armstrong KF, Ball SL. DNA barcodes for biosecurity: invasive species identification, Philosophical Transactions of The Royal Society B Biological Sciences, 360: 1813-1823, 2005.
doi: 10.1098/rstb.2005.1713
[9] Piffaretti J, Vanlerberghe-Masutti F, Tayeh A, Clamens AL, D’Acier AC, Jousselin E. Molecular phylogeny reveals the existence of two sibling species in the aphid pest Brachycaudus helichrysi (Hemiptera: Aphididae), Zoologica Scripta, 41: 266-280, 2012.
doi: 10.1111/j.1463-6409.2012.00531.x
[10] Miller GL, & Foottit RG. The taxonomy of crop pests: The aphids. In: Foottit R, Adler P. eds., Insect Biodiversity: Science and Society. Blackwell Publishing, Oxford. pp. 463-473, 2009.
doi: 10.1002/9781444308211.ch20
[11] Lokeshwari D, Kumar NKK, Manjunatha H. Color polymorphism does not affect species diagnosis of the melon aphid, Aphis gossypii (Hemiptera: Aphididae), Florida Entomologist, 97: 1199-1207, 2014.
doi: 10.1653/024.097.0327
[12] Simon J-C, Peccoud J. Rapid evolution of aphid pests in agricultural environments, Current Opinion in Insect Science, 26: 17-24, 2018.
doi: 10.1016/j.cois.2017.12.009
[13] Kindlmann P, Dixon AF. Modelling population dynamics of aphids and their natural enemies. In Kindlmann P, Dixon AF, Michaud J., eds. Aphid Biodiversity Under Environmental Change, Springer, Dordrecht. pp.1-20, 2010.
doi: 10.1007/978-90-481-8601-3_1
[14]Hosseini-Tabesh B, Sahragard A, Karimi-Malati A. A laboratory and field condition comparison of life table parameters of Aphis gossypii Glover (Hemiptera: Aphididae), Journal of Plant Protection Research, 55: 1-7, 2015.
doi: 10.1515/jppr-2015-0001
[15] McDonald SA, Halbert SE, Tolin SA, Nault BA. Seasonal abundance and diversity of aphids (Homoptera: Aphididae) in a pepper production region in Jamaica, Environmental Entomology, 32: 499-509, 2003.
doi: 10.1603/0046-225X-32.3.499
[16] Blackman RL, Eastop VF. Aphids on the World's Crops: An Identification and Information Guide. 2nd ed. John Wiley and Sons Ltd, Chichester, UK, 2000.
[17] Folmer O, Black M, Hoeh W, Lutz R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates, Molecular Marine Biology and Biotechnology, 3: 294-299, 1994.
[18] Duque-Gamboa DN, Castillo-Cárdenas MF, Hernández LM, Guzmán,YC, Manzano MR, Toro-Perea N. Mitochondrial DNA suggests cryptic speciation in Prodiplosis longifila Gagné (Diptera: Cecidomyiidae) associated with geographic distance and host specialization, Bulletin of Entomological Research, 108: 739-749, 2018.
doi: 10.1017/S0007485317001298
[19] Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0, Molecular Biology and Evolution, 30: 2725-2729, 2013.
doi: 10.1093/molbev/mst197
[20] Hebert PDN, Cywinska A, Ball SL. Biological identifications through DNA barcodes, Proceedings of the Royal Society of London B: Biological Sciences, 270: 313-321, 2003.
doi: 10.1098/rspb.2002.2218
[21]van Velzen R, Weitschek E, Felici G, Bakker FT. DNA barcoding of recently diverged species: Relative performance of matching methods, PloS One, 7: 304-309, 2012.
doi: 10.1371/journal.pone.0030490
[22] Ratnasingham S, Hebert PDN. BOLD: The barcode of life data system, Molecular Ecology Notes, 7: 355-364, 2007.
doi: 10.1111/j.1471-8286.2007.01678.x
[23] Carey JR. Applied demography for biologists with special emphasis on insects. 1st ed. U niversity Press, Oxford, UK, 1993.
doi: 10.1016/0169-5347(94)90043-4
[24] R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2018.
[25] Özgökçe MS, ChiH, Atlıhan R, Kara H. Demography and population projection of Myzus persicae (Sulz.) (Hemiptera: Aphididae) on five pepper (Capsicum annuum L.) cultivars, Phytoparasitica, 46: 153-167, 2018.
doi: 10.1007/s12600-018-0651-0
[26] Amaral D, VenzonM, dos Santos H, Sujii ER, Schmidt JM, Harwood JD. Non-crop plant communities conserve spider populations in chili pepper agroecosystems, Biological Control, 103: 69-77, 2016.
doi: 10.1016/j.biocontrol.2016.07.007
[27] Dixon AFG, Kindlmann P, Leps J, Holman J. Why there are so few species of aphids, especially in the tropics, The American Naturalist, 129: 580-592, 1987.
doi: 10.1086/284659
[28] Duffy C, Fealy R, Fealy RM. An improved simulation model to describe the temperature-dependent population dynamics of the grain aphid, Sitobion avenae, Ecological Modelling, 354: 140-171, 2017.
doi: 10.1016/j.ecolmodel.2017.03.011
[29] Rodriguez N, Michelotto MD, Da Silva RA, Busoli AC. Nymphal development of Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae) on eggplant at different temperatures, Bragantia, 64: 257-262, 2005.
doi: 10.1590/S0006-87052005000200013
[30] Hazell S, Groutides C, Neve B, Blackburn T, Bale J. A comparison of low temperature tolerance traits between closely related aphids from the tropics, temperate zone, and Arctic, Journal of Insect Physiology, 56: 115-122, 2010.
doi: 10.1016/j.jinsphys.2009.08.020
[31] Kersting U, Satar S, Uygun N. Effect of temperature on development rate and fecundity of apterous Aphis gossypii Glover (Hom., Aphididae) reared on Gossypium hirsutum L, Journal of Applied Entomology, 123: 23-27, 1999.
doi: 10.1046/j.1439-0418.1999.00309.x
[32] da Costa JG, Pires EV, Riffel A, Birkett MA, Bleicher E, Sant’Ana AEG. Differential preference of Capsicum spp. cultivars by Aphis gossypii is conferred by variation in volatile semiochemistry, Euphytica, 177: 299-307, 2011.
doi: 10.1007/s10681-010-0250-8
[33] Özder N, Sağlam Ö. The effects of temperature for development time , fecundity and reproduction on some ornamental aphid species, Journal of Central European Agriculture, 14: 627-635, 2013.
doi: 10.5513/JCEA01/14.2.1243
[34] Razmjou J, Moharramipour S, Fathipour Y, Seyed S. Effect of cotton cultivar on performance of Aphis gossypii (Homoptera: Aphididae) in Iran, Journal of Economic Entomology, 99: 1820– 1825, 2006.
doi: 10.1093/jee/99.5.1820
[35] Madahi K, Sahragard A, Hosseini R, Baniameri V. Life history performance of Aphis gossypii (Hemiptera: Aphididae) on six different host plants under microcosm condition, Journal of Entomological Society of Iran, 38: 151-172, 2018.
doi: 10.22117/jesi.2018.121466.1216
[36] Jaquiéry J, Stoeckel S, Larose C, Nouhaud P, Rispe C, Mieuzet L, Bonhomme J, Mahéo F, Legeai F, Gauthier J-P, PrunierLeterme N, Tagu D, Simon J-C. Genetic control of contagious asexuality in the pea aphid, PLoS Genetics, 10: 1-10, 2014.
doi: 10.1371/journal.pgen.1004838
[37] Barbosa LR, Carvalho CF, Auad AM, de Souza, B, Batista EP. Tabelas de esperança de vida e fertilidade de Myzus persicae sobre pimentão em laboratório e casa de vegetação, Bragantia, Campinas, 70: 375-382, 2011.
doi: 10.1590/s0006-87052011000200018
[38] Abdel-Salam AH, Ghanim AA, Hala AKE-S, El-Heneidy AH, Mervat KE-S. Biological and life table parameters of Myzus persicae (Sulz.) (Hemiptera: Aphididae) in relation to host plants and thermal requirements, Mansoura University Journal of Agricultural Sciences, 34: 8251-8262, 2009.
[39] Brault V, Uzest M, Monsion B, Jacquot E, Blanc S. Aphids as transport devices for plant viruses, Comptes Rendus Biologies, 333(6-7): 524-538, 2010.
doi: 10.1016/j.crvi.2010.04.001
[40] Singh K, Singh, R. Effect of temperature on the life history traits of Aphis gossypii Glover (Homoptera: Aphididae) on bottle gourd, Laginaria siceraria (Molina) Standl. (Cucurbitaceae), International Journal of Life Sciences Biotechnology and Pharma Research, 4: 179-183, 2015.
[41] Satar S, Kersting U, Uygun N. Effect of temperature on population parameters of Aphis gossypii Glover and Myzus persicae (Sulzer)(Homoptera: Aphididae) on pepper, Journal for Plant Diseases and Plant Protection, 115: 69-74, 2008.
doi: 10.1007/BF03356241
[42]Yin-jun F, Fen L, Abd Allah MAH, Xiao-qin Y, Min Z, Nicolas D, Xi-wu G. The damage risk evaluation of Aphis gossypii on wheat by host shift and fitness comparison in wheat and cotton, Journal of Integrative Agriculture, 17: 631-639, 2018.
doi: 10.1016/S2095-3119(17)61784-2
[43] Denno RF, McClure MS, Ott JR. Interspecific interactions in phytophagous insects: Competition reexamined and resurrected, Annual Review of Entomology, 40: 297-331, 1995.
doi: 10.1146/annurev.en.40.010195.001501
[44] Guerrieri E, Digilio MC. Aphid-plant interactions: A review, Journal of Plant Interactions, 3: 223-232, 2008.
doi: 10.1080/17429140802567173
[45] Caballero-López B, Bommarco R, Blanco-Moreno JM, Sans FX, Pujade-Villar J, Rundlöf M, Smith HG. Aphids and their natural enemies are differently affected by habitat features at local and landscape scales, Biological Control, 63: 222-229, 2012.
doi: 10.1016/j.biocontrol.2012.03.012
[46]Cui L, Qi H, Yang D, Yuan H Rui C. Cycloxaprid : A novel cisnitromethylene neonicotinoid insecticide to control imidaclopridresistant cotton aphid (Aphis gossypii), Pesticide Biochemistry and Physiology, 132: 1-6, 2016.
doi: 10.1016/j.pestbp.2016.02.005
[47] Zhou K, Huang J, Deng X, van der Werf W, Zhang W, Lu Y, Wu K, Wu F. Effects of land use and insecticides on natural enemies of aphids in cotton: First evidence from smallholder agriculture in the North China Plain, Agriculture, Ecosystems & Environment, 183: 176-184, 2014.
doi: 10.1016/J.AGEE.2013.11.008
[48] Ali A, Desneux N, Lu Y, Wu K. Key aphid natural enemies showing positive effects on wheat yield through biocontrol services in northern China. Agriculture, Ecosystems & Environment, 266: 1-9, 2018.
doi: 10.1016/j.agee.2018.07.012
How to Cite
Manzano, M. R., Tálaga-Taquinas, W., Melo-Cerón, C. I., Lagos-Álvarez, Y. B., Duque-Gamboa, D. N., & Toro-Perea, N. (2020). Identification and life history of aphids associated with chili pepper crops in southwestern Colombia. Universitas Scientiarum, 25(2), 175–200. https://doi.org/10.11144/Javeriana.SC25-2.ialh
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Section
Agricultural entomology