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Functional response and mutual interference in the parasitoid Coptera haywardi (Oglobin) (Hymenoptera: Diapriidae) attacking Anastrepha ludens (Loew) (Diptera: Tephritidae) pupae

Published online by Cambridge University Press:  18 January 2024

Gibran Clemente Open the ORCID record for Gibran Clemente [Opens in a new window] ,
Jorge Toledo Open the ORCID record for Jorge Toledo [Opens in a new window] ,
Gabriela Pérez-Lachaud Open the ORCID record for Gabriela Pérez-Lachaud [Opens in a new window] ,
Javier F. Valle-Mora Open the ORCID record for Javier F. Valle-Mora [Opens in a new window] ,
Pablo Liedo Open the ORCID record for Pablo Liedo [Opens in a new window]  and
Pablo Montoya Open the ORCID record for Pablo Montoya [Opens in a new window]
Gibran Clemente*
Affiliation:
Departamento de Ecología de Artrópodos y Manejo de Plagas, El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto Km 2.5, Tapachula, CP 30700, Chiapas, Mexico
Jorge Toledo
Affiliation:
Departamento de Ecología de Artrópodos y Manejo de Plagas, El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto Km 2.5, Tapachula, CP 30700, Chiapas, Mexico
Gabriela Pérez-Lachaud
Affiliation:
Departamento Conservación de la Biodiversidad, El Colegio de la Frontera Sur (ECOSUR), Avenida Centenario km 5.5, CP 77014 Chetumal, Quintana Roo, Mexico
Javier F. Valle-Mora
Affiliation:
Departamento de Ecología de Artrópodos y Manejo de Plagas, El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto Km 2.5, Tapachula, CP 30700, Chiapas, Mexico
Pablo Liedo
Affiliation:
Departamento de Ecología de Artrópodos y Manejo de Plagas, El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto Km 2.5, Tapachula, CP 30700, Chiapas, Mexico
Pablo Montoya
Affiliation:
Instituto de Biociencias, Universidad Autónoma de Chiapas, Boulevard Akichino S/N, CP 30798, Tapachula, Chiapas, Mexico
*
Corresponding author: Gibran Clemente; Email: gibran.clemente@estudianteposgrado.ecosur.mx
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Abstract

Functional response and mutual interference are important attributes of natural enemies that should be analysed in species with the potential to be used as biological control agents in order to increase the predictive power of the possible benefits and/or consequences of their release in the field. Our main objective was to determine the functional response and mutual interference of Coptera haywardi (Oglobin), a pupal parasitoid of economically important fruit flies (Diptera: Tephritidae). The functional response of C. haywardi on A. ludens pupae corresponded to a type II model, with an attack rate of 0.0134 host pupa/h and a handling time of 1.843 h, which reveals a meticulous selection process of pupal hosts. The effect of mutual interference among foraging females was negatively correlated with increased parasitoid density in the experimental arena, showing a gradual decline in attack rate per individual female. The increase in the number of foraging females also had an impact on the number of oviposition scars per pupa and the number of immature parasitoids per dissected pupa, but not on the percentage of adult emergence or the sex ratio. Our results suggest that C. haywardi could act as a complementary parasitoid in the control of fruit fly pupae, since the random distribution of these pupae in the soil would decrease the possibility of aggregation and mutual interference between foraging females.

Keywords

competitiondensity-dependent superparasitismfruit fliesnatural enemy
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 114 , Issue 1 , February 2024 , pp. 22 - 29
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Copyright © The Author(s), 2024. Published by Cambridge University Press

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References

Aluja, M, Sivinski, J, Rull, J and Hodgson, PJ (2005) Behavior and predation of fruit fly larvae (Anastrepha spp.) (Diptera: Tephritidae) after exiting fruit in four types of habitats in tropical Veracruz, Mexico. Environmental Entomology 34, 1507–1516. Retrieved from https://doi-org.ezproxy.ecosur.mx/10.1603/0046-225X-34.6.1507CrossRefGoogle Scholar
Aluja, M, Sivinski, J, Ovruski, S, Guillén, L, López, M, Cancino, J, Torres-Anaya, A and Gallegos-Chan, G and Ruíz, L (2009) Colonization and domestication of seven species of native New World hymenopterous larval-prepupal and pupal fruit fly (Diptera: Tephritidae) parasitoids. Biocontrol Science and Technology 19, 49–79. https://doi.org/10.1080/09583150802377373CrossRefGoogle Scholar
Baeza-Larios, G, Sivinski, J, Holler, T and Aluja, M (2002) The ability of Coptera haywardi (Ogloblin) (Hymenoptera: Diapriidae) to locate and attack the pupae of the mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), under seminatural conditions. Biological Control 23, 213–218. https://doi.org/10.1006/bcon.2001.1010CrossRefGoogle Scholar
Cancino, J, Liedo, P, Ruiz, L, López, G, Montoya, P, Barrera, JF, Sivinski, J and Aluja, M (2012) Discrimination by Coptera haywardi (Hymenoptera: Diapriidae) of hosts previously attacked by conspecifics or by the larval parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Biocontrol Science and Technology 22, 899–914. Retrieved from https://doi.org/10.1080/09583157.2012.696088CrossRefGoogle Scholar
Cancino, J, Montoya, P, Barrera, JF, Aluja, M and Liedo, P (2014) Parasitism by Coptera haywardi and Diachasmimorpha longicaudata on Anastrepha flies with different fruits under laboratory and field cage conditions. Biological Control 59, 287–295. doi: 10.1007/s10526-014-9571-1Google Scholar
Cancino, J, Pérez, B, Johnson, AC and Reynolds, OL (2019) Parasitoids are choosy: increase in the capacity to discriminate parasitised tephritid pupae by Coptera haywardi. Biocontrol 64, 357–366. doi: 10.1007/s10526-019-09941-5CrossRefGoogle Scholar
De Pedro, L, Beitia, F, Ferrara, F, Asis, J, Sabater-Munoz, B and Tormos, J (2016) Effect of host density and location on the percentage parasitism, fertility and induced mortality of Aganaspis daci (Hymenoptera: Figitidae), a parasitoid of Ceratitis capitata (Diptera: Tephritidae). Crop Protection 92, 160–167. doi: 10.1016/j.cropro.2016.11.007CrossRefGoogle Scholar
DeLong, JP and Uiterwaal, SF (2022) Predator functional responses and the biocontrol of aphids and mites. BioControl 67, 161–172. https://doi.org/10.1007/s10526-021-10127-1CrossRefGoogle Scholar
Fernández-Arhex, V and Corley, JC (2004) Functional response: an overview and experimental guide. Ecología Austral 14, 83–93. Retrieved from http://www.scielo.org.ar/scielo.php?script=sci_arttext&pid=S1667-782X2004000100010&lng=es&tlng=esGoogle Scholar
Fox, J (2005) The R commander: a basic statistics graphical user interface to R. Journal of Statistical Software 14, 1–42. Retrieved from https://www.jstatsoft.org/article/view/v014i09CrossRefGoogle Scholar
Fox, J (2017) Using the R Commander: A Point-and-Click Interface or R. Boca Raton, FL: Chapman and Hall/CRC Press. Retrieved from https://socialsciences.mcmaster.ca/jfox/Books/RCommander/Google Scholar
Fox, J and Bouchet-Valat, M (2019) Rcmdr: R Commander. R package version 2.8–0. Retrieved from https://socialsciences.mcmaster.ca/jfox/Misc/Rcmdr/Google Scholar
Francati, S (2018) Rearing of parasitoid braconid wasp Dinocampus coccinellae in a simplified tritrophic system. Bulletin of Insectology 71, 287–293.Google Scholar
García, JL and Montilla, R (2001) Coptera haywardi Loiácono (Hymenoptera: Diapriidae) a parasitoid of pupae of Anastrepha spp. (Diptera: Tephritidae) in Venezuela. Entomotropica 16, 191–195.Google Scholar
Ghorbani, R, Seraj, AA, Allahyari, H and Farrokhi, S (2019) Functional response of Trichogramma evanescens parasitizing tomato leaf miner, Tuta absoluta on three tomato varieties. Journal of Agricultural Science and Technology 21, 117–127. Retrieved from http://jast.modares.ac.ir/article-23-19862-en.htmlGoogle Scholar
González, PI, Montoya, P, Pérez-Lachaud, G, Cancino, J and Liedo, P (2007) Superparasitism in mass reared Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Biological Control 40, 320–326. https://doi.org/10.1016/j.biocontrol.2006.11.009CrossRefGoogle Scholar
Guillén, L, Aluja, M, Equihua, M and Sivinski, J (2002) Performance of two fruit fly (Diptera: Tephritidae) pupal parasitoids (Coptera haywardi [Hymenoptera: Diapriidae] and Pachycrepoideus vindemiae [Hymenoptera: Pteromalidae]) under different environmental soil conditions. Biological Control 23, 219–227. doi: 10.1006/bcon.2001.1011CrossRefGoogle Scholar
Guleria, P, Sharma, PL, Verma, SC, Chandel, RS and Sharma, N (2020) Functional response of Neochrysocharis formosa to Tuta absoluta. Biocontrol Science and Technology 31, 1–13. Retrieved from https://doi.org/10.1080/09583157.2020.1846163Google Scholar
Hirose, H, Nakamura, T and Takagi, M (1990) Successful biological control: a case study of parasitoid aggregation. In Mackauer, M, Ehler, LE and Roland, J (eds), Critical Issues in Biological Control. Great Britain: Intercept/VHC Publishers, 171–183 pp.Google Scholar
Holling, C (1959) Some characteristics of simple types of predation and parasitism. The Canadian Entomologist 91, 385–398. doi: 10.4039/Ent91385-7CrossRefGoogle Scholar
Juliano, SA (1993) Nonlinear curve fitting: predation and functional response curves. In Scheiner, SM and Gurevitch, J (eds), Design and Analysis of Ecological Experiments. Nueva York: Chapman and Hall, 159–182 pp.Google Scholar
Khan, MH, Khuhro, NH, Awais, M, Memon, RM and Asif, MU (2020) Functional response of the pupal parasitoid, Dirhinus giffardii towards two fruit fly species, Bactrocera zonata and B. cucurbitae. Entomologia Generalis 40, 87–95. doi: 10.1127/entomologia/2020/0878CrossRefGoogle Scholar
Kumar, S, Kashyap, S and Soni, S (2019) The foraging behaviour of Aphelinus asychis Walker (Hymenoptera: Aphelinidae) and Aphidius ervi (Haliday) (Hymenoptera: Braconidae) on Myzus persicae (Sulzer) (Hemiptera: Aphididae). Phytoparasitica 47, 351–360. doi: 10.1007/s12600-019-00735-0CrossRefGoogle Scholar
Li, J, Gong, XM, Chen, YZ, Pan, SY, Dai, YN, Hu, HY and Liu, PC (2022) Effect of maternal age on primary and secondary sex ratios in the ectoparasitoid wasp Pachycrepoideus vindemmiae. Entomologia Experimentalis et Applicata 170, 468–476. doi: 10.1111/eea.13175CrossRefGoogle Scholar
López, P, Rosales, D, Flores, S and Montoya, P (2021) Mutual interference in the mass-reared fruit fly parasitoid, Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Biological Control 66, 649–658. https://doi.org/10.1007/s10526-021-10102-wGoogle Scholar
Luo, S, Li, H, Lu, Y, Zhang, F, Haye, T, Kuhlmann, U and Wu, K (2014) Functional response and mutual interference of Peristenus spretus (Hymenoptera: Braconidae), a parasitoid of Apolygus lucorum (Heteroptera: Miridae). Biocontrol Science and Technology 24, 247–256. http://dx.doi.org/10.1080/09583157.2013.855703CrossRefGoogle Scholar
Martínez-Barrera, OY, Toledo, J, Cancino, J, Liedo, P, Gomez, J, Valle-Mora, J and Montoya, P (2021) Coptera haywardi females discriminate puparia of Anastrepha obliqua treated with Beauveria bassiana. Entomologia Experimentalis et Applicata 169, 976–983. doi: 10.1111/eea.13101CrossRefGoogle Scholar
Merkel, K (2014) Patch exploitation behaviour of the tephritid parasitoid Fopius arisanus, a candidate for the biological control of mango flies (PhD Dissertation). Universitat Bremen, Germany.Google Scholar
Mi, Q, Zhang, J, Haye, T, Zhang, B, Zhao, C, Lei, Y, Li, D and Zhang, F (2021) Fitness and interspecific competition of Trissolcus japonicus and Anastatus japonicus, egg parasitoids of Halyomorpha halys. Biological Control 152, 104461.CrossRefGoogle Scholar
Montoya, P, Liedo, P, Benrey, B, Barrera, JF, Cancino, J and Aluja, M (2000) Functional response and superparasitism by Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Annals of the Entomological Society of America 93, 47–54. Retrieved from https://doi.org/10.1603/0013-8746(2000)093[0047:FRASBD]2.0.CO;2CrossRefGoogle Scholar
Montoya, P, Pérez-Lachaud, G and Liedo, P (2012) Superparasitism in the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) and the implications for mass rearing and augmentative release. Insects 3, 900–911. doi: 10.3390/insects3040900CrossRefGoogle ScholarPubMed
Montoya, P, Gálvez, C and Díaz-Fleischer, F (2019) Host availability affects the interaction between pupal parasitoid Coptera haywardi (Hymenoptera: Diiapridae) and larval-pupal parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Bulletin of Entomological Research 109, 15–23. doi: 10.1017/S0007485318000093CrossRefGoogle ScholarPubMed
Murali-Baskaran, RR, Sharma, KC, Sridhar, J, Jain, L and Kumar, J (2021) Multiple releases of Trichogramma japonicum Ashmead for biocontrol of rice yellow stem borer, Scirpophaga incertulas (Walker). Crop Protection 141, 105471. doi: 10.1016/j.cropro.2020.105471CrossRefGoogle Scholar
Nakamichi, Y, Tuda, M and Wajnberg, E (2020) Intraspecific interference between native parasitoids modified by a non-native parasitoid and its consequence on population dynamics. Ecological Entomology 45, 1263–1271. doi: 10.1111/een.12909CrossRefGoogle Scholar
Núñez-Campero, SR, Ovruski, SM and Aluja, M (2012) Survival analysis and demographic parameters of the pupal parasitoid Coptera haywardi (Hymenoptera: Diapriidae), reared on Anastrepha fraterculus (Diptera: Tephritidae). Biological Control 61, 40–46. doi: 10.1016/j.biocontrol.2011.12.012CrossRefGoogle Scholar
Núñez-Campero, SR, Benitez-Vieyra, S, Gorla, DE and Ovruski, SM (2016) Changes in Diachasmimorpha longicaudata (Hymenoptera: Braconidae) functional response as a consequence of host density choice. Annals of the Entomological Society of America 109, 730–736. doi: 10.1093/aesa/saw045CrossRefGoogle Scholar
Núñez-Campero, SR, Suárez, L, Buonocore-Biancheri, MJ, Cancino, J, Murúa, F, Molina, D, Laría, O, Aluja, M and Ovruski, SM (2020) Host suitability and fitness-related parameters in Coptera haywardi (Hymenoptera: Diapriidae) reared on irradiated Ceratitis capitata (Diptera: Tephritidae) pupae stemming from the tsl Vienna-8 genetic sexing strain. Journal of Economic Entomology 113, 1666–1674. doi: 10.1093/jee/toaa109CrossRefGoogle ScholarPubMed
Okuyama, T (2012) Flexible components of functional responses. Journal of Animal Ecology 81, 185–189. Retrieved from http://www.jstor.org/stable/41331969CrossRefGoogle ScholarPubMed
Poncio, S, Montoya, P, Cancino, J and Nava, ED (2016) Determining the functional response and mutual interference of Utetes anastrephae (Hymenoptera: Braconidae) on Anastrepha obliqua (Diptera: Tephritidae) larvae for mass rearing purposes. Annals of the Entomological Society of America 109, 518–525. Retrieved from https://doi.org/10.1093/aesa/saw031CrossRefGoogle Scholar
Rezaei, M, Talebi, A, Fathipour, Y, Karimzadeh, J and Mehrabadi, M (2019) Foraging behavior of Aphidius matricariae (Hymenoptera: Braconidae) on tobacco aphid, Myzus persicae nicotianae (Hemiptera: Aphididae). Bulletin of Entomological Research 109, 840–848. doi: 10.1017/S0007485319000166CrossRefGoogle ScholarPubMed
Ridout, LM (1981) Mutual interference: behavioural consequences of encounters between adults of the parasitoid wasp Venturia canescens (Hymenoptera: Ichneumonidae). Animal Behaviour 29, 897–903. https://doi.org/10.1016/S0003-3472(81)80026-7CrossRefGoogle Scholar
Salas, GN (2017) Perspectivas del uso del endoparasitoide nativo Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae) para el control biológico de la polilla del tomate Tuta absoluta (Meyrick) (Lepidoptera: Gelechidae) (Tesis Doctoral). Universidad Nacional de La Plata, Argentina, 146 pp.Google Scholar
Savino, V, Coviella, EC and Luna, MG (2012) Reproductive biology and functional response of Dineulophus phtorimaeae, a natural enemy of the tomato moth, Tuta absoluta. Journal of Insect Science 12, 1–14. Retrieved from http://ri.unlu.edu.ar/xmlui/handle/rediunlu/820CrossRefGoogle ScholarPubMed
Sereno, AP, Salvo, A and Battan-Horenstein, M (2016) Trophic interactions between parasitoids and necrophagous flies in Central Argentina. Acta Tropica 162, 229–232. doi: 10.1016/j.actatropica.2016.07.005CrossRefGoogle ScholarPubMed
Sivinski, J, Vulinec, K, Menezes, E and Aluja, M (1998) The bionomics of Coptera haywardi (Ogloblin) (Hymenoptera: Diapriidae) and other pupal parasitoids of tephritid fruit flies (Diptera). Biological Control 11, 193–202. Retrieved from https://doi.org/10.1006/bcon.1997.0597CrossRefGoogle Scholar
Skovgard, H and Nachman, G (2015) Effect of mutual interference on the ability of Spalangia cameroni (Hymenoptera: Pteromalidae) to attack and parasitize pupae of Stomoxys calcitrans (Diptera: Muscidae). Environmental Entomology 44, 1076–1084. doi: 10.1093/ee/nvv096CrossRefGoogle ScholarPubMed
Solomon, ME (1949) The natural control of animal populations. Journal of Animal Ecology 18, 1–35. https://doi.org/10.2307/1578CrossRefGoogle Scholar
Soni, S and Kumar, S (2021) Biological control potential of an aphid parasitoid, Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae) against Brevicoryne brassicae (Linnaeus) (Hemiptera: Aphididae), a pest of oilseed brassicas in India. International Journal of Tropical Insect Science 41, 2361–2372. doi: 10.1007/s42690-020-00408-0CrossRefGoogle Scholar
Stucchi, L, Giménez-Benavides, L and Galeano, J (2019) The role of parasitoids in a nursery-pollinator system: a population dynamics model. Ecological Modelling 396, 50–58. doi: 10.1016/j.ecolmodel.2019.01.011CrossRefGoogle Scholar
Trexler, JC, McCulloch, CE and Travis, J (1988) How can the functional response best be determined?. Oecologia 76, 206–214. Retrieved from https://doi.org/10.1007/BF00379954CrossRefGoogle ScholarPubMed
Tunca, H and Kilincer, N (2009) Effect of superparasitism on the development of the solitary parasitoid Chelonus oculator Panzer (Hymenoptera: Braconidae). Turkish Journal of Agriculture and Forestry 33, 463–468. doi: 10.3906/tar-0807-10Google Scholar
Van Nieuwenhove, G, Bezdjian, LP, Schliserman, P, Aluja, M and Ovruski, SM (2016) Combined effect of larval and pupal parasitoid use for Anastrepha fraterculus (Diptera: Tephritidae) control. Biological Control 95, 94–102. Retrieved from http://dx.doi.org/10.1016/j.biocontrol.2016.01.004CrossRefGoogle Scholar
Visser, EM and Driessen, G (1991) Indirect mutual interference in parasitoids. Netherlands Journal of Zoology 41, 214–227.CrossRefGoogle Scholar
Wang, ZZ, Liu, YQ, Shi, M, Huang, JH and Chen, XX (2019) Parasitoid wasps as effective biological control agents. Journal of Integrative Agriculture 18, 705–715. doi: 10.1016/S2095-3119(18)62078-7CrossRefGoogle Scholar
Yang, XB, Campos-Figueroa, M, Silva, A and Henne, DC (2015) Functional response, prey stage preference, and mutual interference of the Tamarixia triozae (Hymenoptera: Eulophidae) on tomato and bell pepper. Journal of Economic Entomology 108, 414–424. doi: 10.1093/jee/tou048CrossRefGoogle ScholarPubMed
Yazdani, M and Keller, M (2016) The shape of the functional response curve of Dolichogenidea tasmanica (Hymenoptera: Braconidae) is affected by recent experience. Biological Control 96, 63–69. doi: 10.1016/j.biocontrol.2015.05.004CrossRefGoogle Scholar
Zheng, Y, Song, ZW, Zhang, YP and Li, DS (2021) Ability of Spalangia endius (Hymenoptera: Pteromalidae) to parasitize Bactrocera dorsalis (Diptera: Tephritidae) after switching hosts. Insects 12(7), 613. Retrieved from https://doi.org/10.3390/insects12070613CrossRefGoogle ScholarPubMed