Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-20T14:48:58.677Z Has data issue: false hasContentIssue false

Effects of sex ratio on different biological parameters of Engytatus varians (Distant) (Hemiptera: Miridae) adults and their offspring: prey preference for Bactericera cockerelli (Sulcer) (Hemiptera: Triozidae)

Published online by Cambridge University Press:  09 July 2021

Laura Verónica Mena-Mociño
Affiliation:
Instituto de Investigaciones Agropecuarias y Forestales, Universidad Michoacana de San Nicolás de Hidalgo, Tarímbaro, Michoacán, México
Samuel Pineda
Affiliation:
Instituto de Investigaciones Agropecuarias y Forestales, Universidad Michoacana de San Nicolás de Hidalgo, Tarímbaro, Michoacán, México
Ana Mabel Martínez
Affiliation:
Instituto de Investigaciones Agropecuarias y Forestales, Universidad Michoacana de San Nicolás de Hidalgo, Tarímbaro, Michoacán, México
Luis Jesús Palma-Castillo
Affiliation:
Instituto de Investigaciones Agropecuarias y Forestales, Universidad Michoacana de San Nicolás de Hidalgo, Tarímbaro, Michoacán, México
Benjamín Gómez-Ramos
Affiliation:
Tecnológico Nacional de México, Instituto Tecnológico del Valle de Morelia, Morelia, Michoacán, México
Elisa Viñuela
Affiliation:
Protección de Cultivos, Escuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, Universidad Politécnica de Madrid (UPM), Madrid, Spain
José Isaac Figueroa*
Affiliation:
Instituto de Investigaciones Agropecuarias y Forestales, Universidad Michoacana de San Nicolás de Hidalgo, Tarímbaro, Michoacán, México
*
Author for correspondence: José Isaac Figueroa, Email: figueroaji@yahoo.com.mx

Abstract

In the present study, the influence of three sex ratios (1:1, 1:2, and 1:3; female:male) of the mirid Engytatus varians (Distant) (Hemiptera) on different biological parameters and on its offspring was evaluated. The prey preference of different developmental stages of this predator for different nymphal instars (N) of Bactericera cockerelli (Sulcer) (Hemiptera: Triozidae) was also evaluated. The fertility was significantly higher (24 nymphs/female) in the 1:3 sex ratio than in the 1:1 and 1:2 sex ratios (14 and 16 nymphs/female, respectively). The females in the 1:1 and 1:2 sex ratios lived 1.14 and 1.43 days more (27 and 28 days, respectively) than those in the 1:3 sex ratio (26 days). The nymphs derived from the females of the three sex ratios (first filial generation, F1) had five instars and a duration of 17 or 18 days. The ratio of the F1 generation females was not affected by the sex ratio of their parents. In choice tests, independent of whether the preys were placed on a single or multiple tomato (Solanum lycopersicum L.) leaflets, the consumption of females and males and N3, N4, and N5 nymphs of E. varians on B. cockerelli, generally showed the order of N2>N3>N4>N5. In conclusion, the findings revealed in this study can help to improve the rearing methodology for increasing populations of E. varians. In addition, they can serve as a guideline for releasing this predator in times when there is an abundance of early instar nymphs of B. cockerelli.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Abdel-Azim, MM, Vidyasagar, PSPV, Aldosari, SA and Mumtaz, R (2012) Impact of mating frequency on fecundity, fertility and longevity of red palm weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curuclionidae). Journal of Agricultural Science and Technology A2, 520528.Google Scholar
Arnqvist, G and Nilsson, T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour 60, 145164.CrossRefGoogle ScholarPubMed
Ayala, JL, Grillo, H and Vera, ER (1982) Enemigos naturales de Heliothis virescens (Fabricius) (Lepidoptera: Noctuidae) en las provincias centrales de Cuba. Centro Agrícola 9, 314.Google Scholar
Bueno, VHP, Van Lenteren, JC, Lins, JC, Calixto, AM, Montes, FC, Silva, DB, Santiago, LD and Pérez, LM (2013) New records of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) predation by Brazilian hemipteran predatory bugs. Journal of Applied Entomology 137, 2937.CrossRefGoogle Scholar
Castineiras, A (1995) Natural enemies of Bemisia tabaci (Homoptera: Aleyrodidae) in Cuba. Florida Entomologist 78, 538540.CrossRefGoogle Scholar
Chesson, J (1983) The estimation and analysis of preference and its relationship to foraging models. Ecology 64, 12971304.CrossRefGoogle Scholar
Cortés-Piñón, E (2017) Respuesta funcional del depredador Engytatus varians (Distant) (Hemiptera: Miridae) a diferentes densidades de ninfas de Bactericera cockerelli (Sulc.) (Hemiptera: Triozidae) en hojas de jitomate (Tesis de Licenciatura). Instituto Tecnológico del Valle de Morelia, Morelia, Michoacán, México.Google Scholar
Dalin, P, Demoly, T, Kabir, MF and Björkman, C (2011) Global land-use change and the importance of zoophytophagous bugs in biological control: coppicing willows as a timely example. Biological Control 59, 612.CrossRefGoogle Scholar
Fantinou, AA, Perdikis, DC, Labropoulos, PD and Maselou, DA (2009) Preference and consumption of Macrolophus pygmaeus preying on mixed instar assemblages of Myzus persicae. Biological Control 51, 7680.CrossRefGoogle Scholar
Fauvel, G, Malausa, JC and Kaspar, B (1987) Etude en laboratoire des principales characteristiques biologiques de Macrolophus caliginosus (Heteroptera: Miridae). Entomophaga 32, 529543.CrossRefGoogle Scholar
Fedorka, KM and Mousseau, TA (2002) Material and genetic benefits of female multiple mating and polyandry. Animal Behaviour 64, 361367.CrossRefGoogle Scholar
Ferreira, PSF and Henry, TJ (2011) Synopsis and keys to the tribes, genera, and species of Miridae (Hemiptera: Heteroptera) of Minas Gerais, Brazil Part I: Bryocorinae. Zootaxa 2920, 141.CrossRefGoogle Scholar
Ferreira, PSF, Da Silva, ER and Coelho, LBN (2001) Miridae (Heteroptera) fitófagos e predadores de Minas Gerais, Brasil, com ênfase em espécies com potencial econômico. Iheringia Série Zoológica 91, 159169.CrossRefGoogle Scholar
Fitz-Earle, M and Barclay, HJ (1989) Is there an optimal sex ratio for insect mass rearing? Ecological Modelling 45, 205220.CrossRefGoogle Scholar
Foster, SE and Soluk, DA (2006) Protecting more than the wetland: the importance of biased sex ratios and habitat segregation for conservation of the Hine's emerald dragonfly, Somatochlora hineana Williamson. Biological Conservation 127, 158166.CrossRefGoogle Scholar
Franco, K, Jauset, A and Castañe, C (2011) Monogamy and polygamy in two species of mirid bugs: a functional-based approach. Journal of Insect Physiology 57, 307315.CrossRefGoogle ScholarPubMed
Gou, Y, Wang, G, Quandahor, P, Liu, Q and Liu, C (2019) Effects of sex ratio on adult fecundity, longevity and egg hatchability of Bradysia difformis Frey at different temperatures. PLoS ONE 14, 19.CrossRefGoogle ScholarPubMed
Goula, M and Alomar, O (1994) Míridos (Hereroptera Miridae) de interés en el control integrado de plagas en el tomate. Guía para su identificación. Boletín Sanidad Vegetal Plagas 20, 131143.Google Scholar
Hansen, AK, Trumble, JT, Stouthamer, R and Paine, TD (2008) A new huanglongbing species, ‘Candidatus Liberibacter psyllaurous,’ found to infect tomato and potato, is vectored by the Psyllid Bactericera cockerelli (Sulc). Applied and Environmental Microbiology 74, 58625865.CrossRefGoogle Scholar
Hardy, ICW (1994) Sex ratio and mating structure in the parasitoid Hymenoptera. Oikos 69, 320.CrossRefGoogle Scholar
He, C, Shen, DR, Yin, LH, Yuan, SY and Tian, XJ (2017) Effects of different sex ratios on longevity and fecundity of adults of Assara inouei Yamanaka. Plant Protection 43, 6266.Google Scholar
Hernández, LM and Henry, TJ (2010) The plant bugs, or Miridae (Hemiptera: Heteroptera), of Cuba. Pensoft Series Faunistica No. 92, Sofia and Moscow.Google Scholar
Hoagland, DR and Arnon, DI (1950) The water-culture method for growing plants without soil. California. Agricultural Experiment Station. Circular 347.Google Scholar
Hoy, MA (2004) Sex ratio modification by cytoplasmic agents. In Capinera, JL (ed.), Encyclopedia of Entomology, vol. 3. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 19891992.Google Scholar
Illingworth, JF (1937) Observations on the predaceous habits of Cyrtopeltis varians (Dist.) (Hemip.). Proceedings of the Hawaiian Entomological Society 9, 458459.Google Scholar
Jones, RL, Perkins, WD and Sparks, AN (1979) Effects of sex ratios on reproduction by the corn earworm in the laboratory. Annals of the Entomological Society of America 72, 3537.CrossRefGoogle Scholar
Kamimura, Y (2003) Effects of repeated mating and polyandry on the fecundity, fertility and maternal behaviour of female earwigs, Euborellia plebeja. Animal Behaviour 65, 205214.CrossRefGoogle Scholar
Kim, JG, Lee, WH, Yu, YM, Yasunaga-Aok, CH and Jung, SH (2016) Lifecycle, biology, and descriptions of greenhouse biological control agent, Nesidiocoris tenuis (Reuter, 1895) (Hemiptera: Miridae). Journal of the Faculty of Agriculture 61, 313318.Google Scholar
Liefting, LW, Southerland, PW, Ward, LI, Paice, KL, Weir, BS and Clover, GR (2009) A new ‘Candidatus Liberibacter’ species associated with diseases of solanaceous crops. Plant Disease 93, 208214.CrossRefGoogle ScholarPubMed
López, SN, Arce-Rojas, F, Villalba-Velásquez, V and Cagnotti, C (2012) Biology of Tupiocoris cucurbitaceus (Hemiptera: Miridae), a predator of the greenhouse whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) in tomato crops in Argentina. Biocontrol Science and Technology 22, 11071117.CrossRefGoogle Scholar
Lucas, E and Alomar, O (2001) Macrolophus caliginosus (Wagner) as an intraguild prey for the zoophytophagous Dicyphus tamaninii Wagner (Heteroptera: Miridae). Biological Control 20, 147152.CrossRefGoogle Scholar
Madden, AH and Chamberlin, FS (1945) Biology of the tobacco hornworm in the Southern Cigar-Tobacco District. United States Department of Agriculture Washington, D.C Technical Bulletin No. 896.Google Scholar
Martínez, AM, Baena, M, Figueroa, JI, Del Estal, P, Medina, M, Guzmán-Lara, E and Pineda, S (2014) Primer registro de Engytatus varians (Distant) (Hemiptera: Heteroptera: Miridae) en México y su depredación sobre Bactericera cockerelli (Šulc) (Hemiptera: Triozidae): una revisión de su distribución y hábitos. Acta Zoológica Mexicana (nueva serie) 30, 617624.Google Scholar
Mollá, O, Biondi, A, Alonso-Valiente, M and Urbaneja, A (2014) A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. BioControl 59, 175183.CrossRefGoogle Scholar
Morales, ASI, Martínez, AM, Figueroa, JI, Espino, HAM, Chavarrieta, JM, Ortiz, R, Rodríguez-Enríquez, CL and Pineda, S (2013) Parámetros de vida del parasitoide sinovigénico Tamarixia triozae (Hymenoptera: Eulophidae). Revista Colombiana de Entomología 39, 243249.Google Scholar
Morales, SI, Martínez, AM, Viñuela, E, Chavarrieta, JM, Figueroa, JI, Schneider, MI, Tamayo, F and Pineda, S (2018) Lethal and sublethal effects on Tamarixia triozae (Hymenoptera: Eulophidae), an ectoparasitoid of Bactericera cockerelli (Hemiptera: Triozidae), of three insecticides used on solanaceous crops. Journal of Economic Entomology 111, 10481055.CrossRefGoogle Scholar
Nafiu, BS, Dong, H and Cong, B (2014) Principles of biological control in integrated pest management. International Journal of Applied Research and Technology 3, 104116.Google Scholar
Palma-Castillo, LJ, Mena-Mociño, LV, Martínez, AM, Pineda, S, Gómez-Ramos, B, Chavarrieta, JM and Figueroa, JI (2019) Diet and growth parameters of the zoophytophagous predator Engytatus varians (Hemiptera: Miridae). Biocontrol Science and Technology 29, 901911.CrossRefGoogle Scholar
Perdikis, DCH and Lykouressis, DP (2002) Description of the egg and nymphal instar of Macrolophus pygmaeus Rambur (Hemiptera: Miridae). Entomologia Hellenica 14, 3240.CrossRefGoogle Scholar
Pérez-Aguilar, DA, Araújo, MS, Clepf, LP, Martínez, AM, Pineda, S and Carvalho, GA (2018) Lethal and sublethal effects of insecticides on Engytatus varians (Heteroptera: Miridae), a predator of Tuta absoluta (Lepidoptera: Gelechiidae). Ecotoxicology 27, 719728.CrossRefGoogle Scholar
Pérez-Aguilar, DA, Martínez, AM, Viñuela, E, Figueroa, JI, Gómez-Ramos, B, Morales, SI, Tapia, A and Pineda, S (2019) Impact of the zoophytophagous predator Engytatus varians (Hemiptera: Miridae) on Bactericera cockerelli (Hemiptera: Triozidae) control. Biological Control 132, 2935.CrossRefGoogle Scholar
Pineda, S, Medina, M, Figueroa, JI, Henry, TJ, Mena-Mociño, LV, Chavarrieta, JM, Gómez-Ramos, B, Valdez, JM, Lobit, P and Martínez, AM (2016) Life history, diagnosis, and biological aspects of Engytatus varians (Hemiptera: Miridae), a predator of Bactericera cockerelli (Hemiptera: Triozidae). Biocontrol Science and Technology 26, 10731086.CrossRefGoogle Scholar
Pineda, S, Hernández-Quintero, O, Velázquez-Rodríguez, YB, Viñuela, E, Figueroa, JI, Morales, SI and Martínez, AM (2020) Predation by Engytatus varians (Distant) (Hemiptera: Miridae) on Bactericera cockerelli (Sulcer) (Hemiptera: Triozidae) and two Spodoptera species. Bulletin of Entomological Research 110, 270277.CrossRefGoogle ScholarPubMed
Pyke, GH (1984) Optimal foraging theory: a critical review. Annual Review of Ecology Systematics 15, 523575.CrossRefGoogle Scholar
Ramírez-Ahuja, ML, Rodríguez-Leyva, E, Lomeli-Flores, JR, Torres-Ruiz, A and Guzmán-Franco, AW (2017) Evaluating combined use of a parasitoid and a zoophytophagous bug for biological control of the potato psyllid, Bactericera cockerelli. Biological Control 106, 915.CrossRefGoogle Scholar
Sheldon, BS and West, SA (2002) Sex ratios. In Pagel, M (ed.), Encyclopedia of Evolution, vol. 2. Oxford, England: Oxford University Press, pp. 10401044.Google Scholar
Silva, CCA, Laumann, RA, Cavalcante-Ferreira, JB, Blassioli-Moraes, MC, Borges, M and Cokl, A (2012) Reproductive biology, mating behavior, and vibratory communication of the brown-winged stink bug, Edessa meditabunda (Fabr.) (Heteroptera: Pentatomidae). Psyche 2012, 19.CrossRefGoogle Scholar
Silva, DB, Bueno, VHP, Montes, FC and van Lenteren, JC (2016) Population growth of three mirid predatory bugs feeding on eggs and larvae of Tuta absoluta on tomato. Biological Control 61, 545553.Google Scholar
Simmons, LW (2001) The evolution of polyandry: an examination of the genetic incompatibility and good-sperm hypotheses. Journal of Evolutionary Biology 14, 585594.CrossRefGoogle Scholar
Slansky, F and Rodriguez, JG (1987) Nutritional ecology of insects, mites, spiders and related invertebrates: an overview. In Slansky, F and Rodriguez, JG (eds), Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates. New York: Wiley, pp. 169.Google Scholar
Urbaneja, A, Tapia, G and Stansly, P (2005) Influence of host plant and prey availability on developmental time and survivorship of Nesidiocoris tenuis (Het.: Miridae). Biocontrol Science and Technology 15, 513518.CrossRefGoogle Scholar
Valderrama, K, Granobles, J, Valencia, E and Sánchez, M (2007) Nesidiocoris tenuis (Hemiptera: Miridae) depredador en el cultivo de tabaco (Nicotiana tabacum). Revista Colombiana de Entomología 33, 141145.Google Scholar
van Dijken, MJ, van Stratum, P and van Alphen, JJM (1993) Superparasitism and sex ratio in the solitary parasitoid Epidinocarsis lopezi. Entomologia Experimentalis et Applicata 68, 5158.CrossRefGoogle Scholar
van Lenteren, JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57, 120.CrossRefGoogle Scholar
van Lenteren, JC, Hemerik, L, Lins, JC Jr and Bueno, VHP (2016) Functional responses of three neotropical mirid predators to eggs of Tuta absoluta on tomato. Insects 7, 110.CrossRefGoogle ScholarPubMed
Wedell, N, Wiklund, C and Cook, PA (2002) Monoandry and polyandry as alternative lifestyles in butterfly. Behavioral Ecology 13, 450455.CrossRefGoogle Scholar
Wehi, PM, Nakagawa, S, Trewick, SA and Mongan-Richards, M (2011) Does predation result in adult sex ratio skew in a sexually dimorphic insect genus? Journal of Evolutionary Biology 24, 23212328.CrossRefGoogle Scholar
Wei, YJ (2008) Studies of life history and some aspects of field biology and ecology of Nysius huttoni White (Hemiptera: Lygaeidae). Journal of the Royal Society of New Zealand 38, 149162.CrossRefGoogle Scholar
West, SA and Sheldon, BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295, 16851688.CrossRefGoogle ScholarPubMed
Wheeler, AG Jr (2001) Biology of the Plant Bugs (Hemiptera: Miridae). Pests, Predators, Opportunists. Cornell University Press, Ithaca, New York. 507 pp.Google Scholar
Wiklund, C, Kaitala, A, Lindfors, V and Abeniu, J (1993) Polyandry and its effect on female reproduction in the green-veined white butterfly (Pieris napi L.). Behavioral Ecology and Sociobiology 33, 2533.CrossRefGoogle Scholar
Williams, T, Arredondo-Bernal, HC and Rodríguez-del-Bosque, LA (2013) Biological pest control in Mexico. Annual Review of Entomology 58, 119140.CrossRefGoogle ScholarPubMed