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Fertility life table and biology of Tetrastichus giffardianus (Hymenoptera: Eulophidae) in the larvae of Ceratitis capitata (Diptera: Tephritidae)

Published online by Cambridge University Press:  20 August 2020

Elania Clementino Fernandes Open the ORCID record for Elania Clementino Fernandes [Opens in a new window] ,
Mariana Macedo Souza Open the ORCID record for Mariana Macedo Souza [Opens in a new window] ,
Dori Edson Nava Open the ORCID record for Dori Edson Nava [Opens in a new window] ,
Janisete Gomes Silva Open the ORCID record for Janisete Gomes Silva [Opens in a new window]  and
Elton Lucio Araujo Open the ORCID record for Elton Lucio Araujo [Opens in a new window]
Elania Clementino Fernandes*
Affiliation:
Universidade Federal Rural do Semi-Árido (UFERSA), Av. Francisco Mota, 572, Costa e Silva, 59625-900, Mossoró, RN, Brazil
Mariana Macedo Souza
Affiliation:
Universidade Federal Rural do Semi-Árido (UFERSA), Av. Francisco Mota, 572, Costa e Silva, 59625-900, Mossoró, RN, Brazil
Dori Edson Nava
Affiliation:
Embrapa Clima Temperado, Rod. BR-392, km 78, 96010-971, Pelotas, RS, Brazil
Janisete Gomes Silva
Affiliation:
Universidade Estadual de Santa Cruz (UESC), Rod. Jorge Amado, km 16, 56629-000, Ilhéus, BA, Brazil
Elton Lucio Araujo
Affiliation:
Universidade Federal Rural do Semi-Árido (UFERSA), Av. Francisco Mota, 572, Costa e Silva, 59625-900, Mossoró, RN, Brazil
*
Author for correspondence: Elania Clementino Fernandes, Email: elania.fernandes@ufersa.edu.br
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Abstract

Tetrastichus giffardianus is a gregarious koinobiont endoparasitoid of tephritids, including Ceratitis capitata, which is one of the most important fruit pests worldwide. The objective of this study was to evaluate the effect of constant temperatures on the biology and development of the egg-adult period of T. giffardianus in larvae/pupae of C. capitata to construct a fertility life table. The study was carried out in climatic chambers at constant temperatures of 15, 20, 25, 30, and 35 ± 1°C, 70 ± 10% relative humidity and a photophase of 12 h. Complete egg and larval development occurred only at temperatures of 20, 25, and 30°C. The mean longevity of males and females was inversely proportional to temperature. The time of development of the pre-imaginal period was influenced by temperature and ranged from 41 days at 20°C to 11 days at 25°C. The best T. giffardianus performance occurred at 25°C when the intrinsic rate of increase was 0.21, the mean generation time was 20.43 days, the time required to double the population was 3.33 days, and the finite rate of population increase (λ) was 1.23. The results of this study provided information for the establishment of mass rearing and an evaluation of the adaptability of T. giffardianus to different environments, which is necessary for the use of this parasitoid in the biological control of tephritid pests, particularly C. capitata.

Keywords

Biological controldevelopmentfruit fliesparasitoid
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 2 , April 2021 , pp. 182 - 189
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Albajes, R and Santiago-Alvarez, C (1980) Influencia de la temperatura en el desarollo de Ceratitis capitata (Wied.). Anales, INIA, Serie Agricola 13, 183–190.Google Scholar
Appiah, EF, Ekesi, S, Salifu, D, Afreh-Nuamah, K, Obeng-Ofori, D, Khamis, F and Mohamed, SA (2013) Effect of temperature on immature development and longevity of two introduced opiine parasitoids on Bactrocera invadens. Journal of Applied Entomology 137, 571–579.CrossRefGoogle Scholar
Araujo, EL, Fernandes, EC, Silva, RIR, Ferreira, ADCL and Costa, VA (2015) Parasitoids (Hymenoptera) of fruit flies (Diptera: Tephritidae) in semiarid ambient, in the state of Ceará, Brasil. Revista Brasileira de Fruticultura 37, 610–616.CrossRefGoogle Scholar
Casas, J, Pincebourde, S, Mandon, N, Vannier, F, Poujol, R and Giron, D (2005) Lifetime nutrient dynamics reveal simultaneous capital and income breeding in a parasitoid. Ecology 86, 545–554.CrossRefGoogle Scholar
Costa, VA, Araujo, EL, Guimarães, JA, Nascimento, AS and Lasalle, J (2005) Redescoberta de Tetrastichus giffardianus (Hymenoptera: Eulophidae) após 60 anos da sua introdução no Brasil. Arquivos do Instituto Biológico 72, 539–541.Google Scholar
De Pedro, L, Beitia, F, Sabater-Muñoz, B, Asís, JD and Tormos, J (2016) Effect of temperature on the developmental time, survival of immatures and adult longevity of Aganaspis daci (Hymenoptera: Figitidae), a natural enemy of Ceratitis capitata (Diptera: Tephritidae). Crop Protection 85, 17–22.CrossRefGoogle Scholar
Fernandes, EC, Araujo, EL, Souza, IM, Souza, MM and Nunes, GH (2019 a) Development and morphological characterization of the immature stages of Tetrastichus giffardianus Silvestri (Hymenoptera: Eulophidae). Revista Brasileira de Entomologia 63, 262–267.CrossRefGoogle Scholar
Fernandes, EC, Souza, MM, Alves, MI, Felipe, AGN and Araujo, EL (2019 b) Rearing technique and demographic parameters of Tetrastichus giffardianus Silvestre (Hymenoptera: Eulophidae). Semina: Ciências Agrárias 40, 2201–2208.Google Scholar
Garcia, FRM and Ricalde, MP (2013) Augmentative biological control using parasitoids for fruit fly management in Brazil. Insects 4, 55–70.CrossRefGoogle Scholar
Gonçalves, RS, Nava, DE, Andreazza, F, Lisbôa, H, Nunes, AM, Grützmacher, AD, Valgas, RA, Maia, AHN and Pazianotto, RAA (2014) Effect of constant temperatures on the biology, life table, and thermal requirements of Aganaspis pelleranoi (Hymenoptera: Figitidae), a parasitoid of Anastrepha fraterculus (Diptera: Tephritidae). Environmental Entomology 43, 491–500.CrossRefGoogle Scholar
Gonçalves, RS, Andreazza, F, Lisbôa, H, Grützmacher, AD, Valgas, RA, Manica-Berto, R, Nörnberg, SD and Nava, DE (2016) Basis for the development of a rearing technique of Aganaspis pelleranoi (Hymenoptera: Figitidae) in Anastrepha fraterculus (Tephritidae: Diptera). Journal of Economic Entomology 109, 1094–1101.CrossRefGoogle Scholar
Groth, MZ, Loeck, AE, Nornberg, SD, Bernardi, D and Nava, DE (2017) Biology and thermal requirements of Fopius arisanus (Sonan, 1932) (Hymenoptera: Braconidae) reared on Ceratitis capitata eggs (Wiedemann) (Diptera: Tephritidae). Neotropical Entomology 46, 554–560.CrossRefGoogle Scholar
Hance, T, van Baaren, J, Vernon, P and Boivin, G (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annual Review of Entomology 52, 107–126.CrossRefGoogle Scholar
Harvey, JA, Poelman, EH and Tanaka, T (2013) Intrinsic inter- and intraspecific competition in parasitoid wasps. Annual Review of Entomology 58, 333–351.CrossRefGoogle ScholarPubMed
Heimpel, GE and Lundgren, JG (2000) Sex ratios of commercially reared biological control agents. Biological Control 19, 77–93.CrossRefGoogle Scholar
Jaworski, T and Hilszczański, J (2013) The effect of temperature and humidity changes on insects’ development their impact on forest ecosystems in the expected climate change. Forest Research Papers 74, 345–355.CrossRefGoogle Scholar
Jervis, MA, Ellers, J and Harvey, JA (2008) Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annual Review of Entomology 53, 361–385.CrossRefGoogle ScholarPubMed
Loni, A (1997) Developmental rate of Opius concolor (Hym.: Braconidae) at various constant temperatures. Entomophaga 42, 359–366.CrossRefGoogle Scholar
Maia, AHN, Luiz, AJB and Campanhola, C (2000) Statistical inference on associated fertility life table parameters using jackknife technique: computational aspects. Journal of Economic Entomology 93, 511–518.CrossRefGoogle Scholar
Meirelles, RN, Redaelli, LR and Orique, CB (2013) Comparative biology of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) reared on Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae). Florida Entomologist 96, 412–418.CrossRefGoogle Scholar
Meyer, JS, Ingersoll, CG, McDonald, LL and Boyce, MS (1986) Estimating uncertainty in population growth rates: jackknife vs. Bootstrap techniques. Ecology 67, 1156–1166.CrossRefGoogle Scholar
Mirondis, GK and Savopoulou-Soultani, M (2008) Development, survivorship, and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) under constant and alternating temperatures. Environmental Entomology 37, 16–28.CrossRefGoogle Scholar
Mohamed, SA, Wharton, RA, Mérey, G and von and Schulthess, F (2006) Acceptance and suitability of different host stages of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) and seven other tephritid fruit fly species to Tetrastichus giffardii Silvestri (Hymenoptera: Eulophidae). Biological Control 39, 262–271.CrossRefGoogle Scholar
Mohamed, SA, Ramadam, MM and Ekesi, S (2016) In and out of Africa: Parasitoids used for biological control of fruit flies. In Ekesi S, Mohamed SA and De Meyer M (eds), Fruit Fly Research and Development in Africa – Towards a Sustainable Management Strategy to Improve Horticulture. Cham, Switzerland: Springer International Publishing, pp. 325–368.CrossRefGoogle Scholar
Nyamukondiwa, C, Weldon, CW, Chown, SL, le Roux, PC and Terblanche, JS (2013) Thermal biology, population fluctuations and implications of temperature extremes for the management of two globally significant insect pests. Journal of Insect Physiology 59, 1199–1211.CrossRefGoogle ScholarPubMed
Ovruski, S, Aluja, M, Sivinski, J and Wharton, R (2000) Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: diversity, distribution, taxonomic status and their use in fruit fly biological control. Integrated Pest Management Reviews 5, 81–107.CrossRefGoogle Scholar
Pedigo, LP and Zeiss, RM (1996) Constructing life table for insect populations. In Pedigo, LP (ed), Analyses in Insect Ecology and Management. Iowa City: Iowa State University Press, pp. 75–105.Google Scholar
Poncio, S, Nunes, AM, Gonçalves, RS, Lisboa, H, Manica-Berto, R, Garcia, MS and Nava, DE (2016) Biology of Doryctobracon brasiliensis at different temperatures: development of life table and determining thermal requirements. Journal of Applied Entomology 140, 775–785.CrossRefGoogle Scholar
Purcell, MF, Nieuwenhoven, A and Batchelor, MA (1996) Bionomics of Tetrastichus giffardianus (Hymenoptera: Eulophidae): an endoparasitoid of tephritid fruit flies. Environmental Entomology 25, 198–206.CrossRefGoogle Scholar
R Development Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Ramadan, MM and Wong, TTY (1990) Biological observations on Tetrastichus giffardianus a gregarious endoparasitoid of the Mediterranean fruit fly and the oriental fruit fly (Diptera: Tephritidae). Proceedings Hawaiian Entomological Society 30, 59–62.Google Scholar
Ricalde, MP, Nava, DE, Loeck, AE and Donatti, MG (2012) Temperature-dependent development and survival of Brazilian populations of the Mediterranean fruit fly, Ceratitis capitata, from tropical, subtropical and temperate regions. Journal of Insect Science 12, 1–11.CrossRefGoogle ScholarPubMed
Sagarra, LA, Vincent, C and Stewart, RK (2001) Body size as an indicator of parasitoid quality in male and female Anagyrus kamali (Hymenoptera: Encyrtidae). Bulletin of Entomological Research 91, 363–367.CrossRefGoogle Scholar
Sime, KR, Daane, KM, Nadel, H, Funk, CS, Messing, RH, Andrews, JW, Johnson, MW and Pickett, CH (2006) Diachasmimorpha longicaudata and D. kraussii (Hymenoptera: Braconidae), potential parasitoids of the olive fruit fly. Biocontrol Science and Technology 16, 169–179.CrossRefGoogle Scholar
Snart, CJP, Kapranas, A, Williams, H, Barrett, DA and Hardy, ICW (2018) Sustenance and performance: nutritional reserves, longevity, and contest outcomes of fed and starved adult parasitoid wasps. Frontiers in Ecology and Evolution 6, 1–12.CrossRefGoogle Scholar
Stacconi, MVR, Panel, A, Baser, NC, Pantezzi, T and Anfora, G (2017) Comparative life history traits of indigenous Italian parasitoids of Drosophila suzukii and their effectiveness at different temperatures. Biological Control 112, 20–27.CrossRefGoogle Scholar
Szyniszewska, AM and Tatem, AJ (2014) Global assessment of seasonal potential distribution of Mediterranean fruit fly, Ceratitis capitata (Diptera: tephritidae). PLoS ONE 9, 1–13.CrossRefGoogle Scholar
Vargas, RI, Ramadan, M, Hussain, T, Mochizuki, N, Bautista, RC and Stark, JD (2002) Comparative demography of six fruit fly (Diptera: Tephritidae) parasitoids (Hymenoptera: Braconidae). Biological Control 25, 30–40.CrossRefGoogle Scholar
Wang, XG, Kaçar, G, Biondi, A and Daane, KM (2016 a) Life-history and host preference of Trichopria drosophilae, a pupal parasitoid of spotted wing drosophila. BioControl 61, 387–397.CrossRefGoogle Scholar
Wang, XG, Kaçar, G, Biondi, A and Daane, KM (2016 b) Foraging efficiency and outcomes of interactions of two pupal parasitoids attacking the invasive spotted wing drosophila. Biological Control 96, 64–71.CrossRefGoogle Scholar
Wiman, NG, Walton, VM, Dalton, DT, Anfora, G, Burrack, HJ, Chiu, JC, Daane, KM, Grassi, A, Miller, B, Tochen, S, Wang, XG and Ioriatti, C (2014) Integrating temperature-dependent life table data into a matrix projection model for drosophila suzukii population estimation. PLoS ONE 9, 106909.CrossRefGoogle ScholarPubMed
Zuo, W, Moses, ME, West, GB, Hou, C and Brown, JH (2012) A general model for effects of temperature on ectotherm ontogenetic growth and development. Proceedings of the Royal Society B: Biological Sciences 279, 1840–1846.CrossRefGoogle ScholarPubMed