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Superparasitism and fitness parameters in three native wasp parasitoids (Braconidae: Opiinae) of the Mexican fruit fly, Anastrepha ludens (Diptera: Tephritidae)

Published online by Cambridge University Press:  17 September 2021

Amanda Ayala Open the ORCID record for Amanda Ayala [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] ,
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]
Amanda Ayala*
Affiliation:
El Colegio de la Frontera Sur, Agricultura, Sociedad y Ambiente, Carretera Antiguo Aeropuerto Km 2.5, Tapachula, Chiapas, 30700, México Programa Moscafrut SENASICA-SADER, Camino a los Cacaotales S/N, Metapa de Domínguez, Chiapas, 30860, México
Jorge Toledo
Affiliation:
El Colegio de la Frontera Sur, Agricultura, Sociedad y Ambiente, Carretera Antiguo Aeropuerto Km 2.5, Tapachula, Chiapas, 30700, México
Gabriela Pérez-Lachaud
Affiliation:
El Colegio de la Frontera Sur, Conservación de la Biodiversidad, Avenida Centenario Km 5.5, Chetumal, Quintana Roo, 77014, México
Pablo Liedo
Affiliation:
El Colegio de la Frontera Sur, Agricultura, Sociedad y Ambiente, Carretera Antiguo Aeropuerto Km 2.5, Tapachula, Chiapas, 30700, México
Pablo Montoya
Affiliation:
Programa Moscafrut SENASICA-SADER, Camino a los Cacaotales S/N, Metapa de Domínguez, Chiapas, 30860, México
*
Author for correspondence: Amanda Ayala, Email: [email protected]
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Abstract

Knowledge on reproductive strategies and host use in insect parasitoids is fundamental for biological control purposes. Superparasitism and multiparasitism, oviposition in a previously parasitized host by a female of the same or different species, respectively, may impact pest management decisions. Our objective was to determine the occurrence of superparasitism and multiparasitism in three species of native larval−pupal solitary endoparasitoids that attack Anastrepha Shiner species (Diptera: Tephritidae) in the Neotropical region, and the possible effect on offspring fitness parameters. Doryctobracon crawfordi (Viereck), Utetes anastrephae (Viereck), and Opius hirtus (Fischer) occur in sympatry in Mexico, and are currently under consideration for use as biocontrol agents. Experiments were conducted under laboratory conditions with females acting alone (self-superparasitism), females in groups of the same species (conspecific superparasitism), and females in mixed groups (multiparasitism). Our results showed that self-superparasitism is an uncommon strategy in the three native species and is rare under conditions of intraspecific competition. In the case of multiparasitism, a higher number of immature stages of U. anastrephae was observed, compared to those of D. crawfordi and O. hirtus. However, it is not clear yet if this was due to some adult female trait or to the competitive ability of the larvae. We conclude that most females of the native species studied appeared to avoid superparasitism, specifically when acting alone, suggesting a high discrimination ability, which is probably a result of a close relationship and evolutionary history with Anastrepha hosts.

Keywords

Doryctobracon crawfordimultiparasitismOpiinaeOpius hirtusself-superparasitismUtetes anastrephae
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 2 , April 2022 , pp. 253 - 260
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Aluja, M, Sivinski, J, Ovruski, S, Guillen, L, Lopez, M, Cancino, J, Torres Anaya, A, Gallegos-Chan, G and Ruiz, 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.CrossRefGoogle Scholar
Ayala, A, Martinez, AM, Figueroa, I, Pineda, S, Miranda, M, Liedo, P and Montoya, P (2014) Superparasitism strategies by a native and an exotic parasitoid species attacking the Mexican fruit fly, Anastrepha ludens (Diptera: Tephritidae). Biocontrol Science and Technology 24, 925–935.CrossRefGoogle Scholar
Ayala, A, Pérez-Lachaud, G, Toledo, J, Liedo, P and Montoya, P (2018) Host acceptance by three native braconid parasitoid species attacking larvae of the Mexican fruit fly, Anastrepha ludens (Diptera, Tephritidae). Journal of Hymenoptera Research 63, 33–49.CrossRefGoogle Scholar
Bakker, K, van Alphen, JJM, van Batenburg, FHD, van der Hoeven, N, Nell, HW, van Strien-van Liempt, WTFH and Turlings, TCJ (1985) The function of host discrimination and superparasitization in parasitoids. Oecologia 67, 572–576.CrossRefGoogle ScholarPubMed
Bográn, CE, Heinz, KM and Ciomperlik, MA (2002) Interspecific competition among insect parasitoids: field experiments with whiteflies as hosts in cotton. Ecology 83, 653–668.CrossRefGoogle Scholar
Charnov, EL and Stephens, DW (1988) On the evolution of host selection in solitary parasitoids. The American Naturalist 132, 707–722.CrossRefGoogle Scholar
Cicero, L, Sivinski, J, Rull, J and Aluja, M (2011) Effect of larval host food substrate on egg load dynamics, egg size and adult female size in four species of braconid fruit fly (Diptera: Tephritidae) parasitoids. Journal of Insect Physiology 57, 1471–1479.CrossRefGoogle ScholarPubMed
Cusumano, A, Peri, E and Colazza, S (2016) Interspecific competition/facilitation among insect parasitoids. Current Opinion in Insect Science 14, 12–16.CrossRefGoogle ScholarPubMed
Darrouzet, E, Imbert, E and Chevrier, C (2003) Self-superparasitism consequences for offspring sex ratio in the solitary ectoparasitoid Eupelmus vuilleti. Entomologia Experimentalis et Applicata 109, 167–171.CrossRefGoogle Scholar
FAO/IAEA/USDA (2019) Product Quality Control for Sterile Mass-Reared and Released Tephritid Fruit Flies, Version 7.0. Vienna, Austria: International Atomic Energy Agency. 148 pp.Google Scholar
García-Medel, D, Sivinski, J, Díaz-Fleischer, F, Ramírez-Romero, R and Aluja, M (2007) Foraging behavior by six fruit fly parasitoids (Hymenoptera: Braconidae) released as single- or multiple-species cohorts in field cages: influence of fruit location and host density. Biological Control 43, 12–22.CrossRefGoogle Scholar
Gauthier, N and Monge, JP (1999) Could the egg itself be the source of the oviposition deterrent marker in the ectoparasitoid Dinarmus basalis? Journal of Insect Physiology 45, 393–400.CrossRefGoogle ScholarPubMed
Godfray, HCJ (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton: Princeton University Press.CrossRefGoogle 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.CrossRefGoogle Scholar
González, PI, Montoya, P, Pérez-Lachaud, G, Cancino, J and Liedo, P (2010) Host discrimination and superparasitism in wild and mass-reared Diachasmimorpha longicaudata (Hym.: Braconidae) females. Biocontrol Science and Technology 20, 137–148.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
Hernández-Ortíz, V, Perez-Alonso, R and Wharton, RA (1994) Native parasitoids associated with the genus Anastrepha (Diptera: Tephritidae) in Los Tuxtlas, Veracruz, México. Entomophaga 39, 171–178.CrossRefGoogle Scholar
Hubbard, SF, Marris, G, Reynolds, A and Rowe, GW (1987) Adaptive patterns in the avoidance of superparasitism by solitary parasitic wasps. Journal of Animal Ecology 56, 387–401.CrossRefGoogle Scholar
King, BH (1993) Sex ratio manipulation by parasitoid wasps. In Wrensch, DL and Ebbert, MA (eds), Evolution and Diversity of Sex Ratio in Insects and Mites. New York: Chapman & Hall, pp. 418–441.CrossRefGoogle Scholar
Lawrence, PO, Greany, PD, Nation, JL and Baranowski, RM (1978) Oviposition behavior of Biosteres longicaudatus, a parasite of the Caribbean fruit fly, Anastrepha suspensa. Annals of the Entomological Society of America 71, 253–256.CrossRefGoogle Scholar
Lebreton, S, Chevrier, C and Darrouzet, E (2010) Sex allocation strategies in response to conspecifics’ offspring sex ratio in solitary parasitoids. Behavioral Ecology 21, 107–112.CrossRefGoogle Scholar
Lee, ET and Wang, JW (2003) Statistical Methods for Survival Data Analysis. New York, NY: Wiley.CrossRefGoogle Scholar
López, M, Aluja, M and Sivinski, J (1999) Hymenopterous larval–pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in Mexico. Biological Control 15, 119–129.CrossRefGoogle Scholar
Mackauer, M. (1990) Host discrimination and larval competition in solitary endoparasitoids. In Mackauer, M, Ehler, LE and Roland, J (eds), Critical Issues in Biological Control, Andover: Intercept, pp. 41–62.Google Scholar
Mackauer, M, Bai, B, Chow, A and Danyk, T (1992) Asymmetric larval competition between two species of solitary parasitoid wasps: the influence of superparasitism. Ecological Entomology 17, 233–236.CrossRefGoogle Scholar
May, RM and Hassell, MP (1981) The dynamics of multiparasitoid-host interactions. The American Naturalist 117, 234–261.CrossRefGoogle Scholar
Montoya, P, Liedo, P, Benrey, B, Cancino, J, Barrera, JF, Sivinski, J and Aluja, M (2000) Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biological Control 18, 216–224.CrossRefGoogle Scholar
Montoya, P, Benrey, B, Barrera, JF, Zenil, M, Ruiz, L and Liedo, P (2003) Oviposition behavior and conspecific host discrimination in Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a fruit fly parasitoid. Biocontrol Science Technology 13, 683–690.CrossRefGoogle Scholar
Montoya, P, Cancino, J, Pérez-Lachaud, G and Liedo, P (2011) Host size, superparasitism and sex ratio in mass-reared Diachasmimorpha longicaudata, a fruit fly parasitoid. BioControl 56, 11–17.CrossRefGoogle Scholar
Montoya, P, Ruiz, L, Pérez-Lachaud, G, Cancino, J and Liedo, P (2013) Field superparasitism by Diachasmimorpha longicaudata attacking Anastrepha spp. larvae on mango fruits. Biological Control 64, 160–165.CrossRefGoogle Scholar
Moreau, SJM and Asgari, S (2015) Venom proteins from parasitoid wasps and their biological functions. Toxins 7, 2385–2412.CrossRefGoogle ScholarPubMed
Murillo, FD, Liedo, P, Nieto-López, MG, Cabrera-Mireles, H, Barrera, JF and Montoya, P (2016) First instar larvae morphology of Opiinae (Hymenoptera: Braconidae) parasitoids of Anastrepha (Diptera: Tephritidae) fruit flies. Implications for interspecific competition. Arthropod Structure & Development 45, 294–300.CrossRefGoogle ScholarPubMed
Nelson, JM and Roitberg, BD (1995) Flexible patch time allocation by the leafminer parasitoid, Opius dimidiatus. Ecological Entomology 20, 245–252.CrossRefGoogle Scholar
Orozco-Dávila, D, Quintero, L, Hernández, E, Solís, E, Artiaga, T, Hernández, R and Montoya, P (2017) Mass rearing and sterile insect releases for the control of Anastrepha spp. (Diptera: Tephritidae) pests in Mexico – a review. Entomologia Experimentalis et Applicata 164, 76–187.CrossRefGoogle Scholar
Outreman, Y and Pierre, JS (2005) Adaptive value of host discrimination in parasitoids: when host defenses are very costly. Behavioural Process 70, 93–103.CrossRefGoogle Scholar
Outreman, Y, Le Ralec, A, Plantegenest, M, Chaubet, B and Pierre, JS (2001) Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. Journal of Insect Physiology 47, 339–348.CrossRefGoogle Scholar
Ovruski, S, Aluja, M, Sivinski, J and Wharton, RA (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
Ovruski, S, Colin, C, Soria, A, Oroño, LE and Schliserman, P (2003) Introducción y producción en laboratorio de Diachasmimorpha tryoni y Diachasmimorpha longicaudata (Hymenoptera: Braconidae) para el control biológico de Ceratitis capitata (Diptera: Tephritidae) en la Argentina. Revista de la Sociedad Entomologica de Argentina 62, 49–59.Google Scholar
Ovruski, S, Wharton, RA, Schliserman, P and Aluja, M (2005) Abundance of Anastrepha fraterculus (Diptera: Tephritidae) and its associated native parasitoids (Hymenoptera) in “feral” guavas growing in the endangered northernmost Yungas forests of Argentina with an update on the taxonomic status of Opiinae parasitoids previously reported in this country. Environmental Entomology 34, 807–818.CrossRefGoogle Scholar
Pijls, JWAM, Hofker, KD, van Staalduinen, MJ and van Alphen, JJM (1995) Interspecific host discrimination and competition in Apoanagyrus (Epidinocarsis) lopezi and A. (E.) diversicornis, parasitoids of the cassava mealybug Phenacoccus manihoti. Ecological Entomology 20, 326–332.CrossRefGoogle Scholar
Poelman, EH, Gols, R, Gumovsky, AV, Cortesero, AM, Dicke, M and Harvey, JA (2014) Food plant and herbivore host species affect the outcome of intrinsic competition among parasitoid larvae. Ecological Entomology 39, 693–702.CrossRefGoogle Scholar
Poncio, S, Montoya, P, Cancino, J and Nava, DE (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.CrossRefGoogle Scholar
Pschorn-Walcher, H (1987) Interspecific competition between the principal larval parasitoids of the pine sawfly, Neodiprion sertifer (Geoff.) (Hym.: Diprionidae). Oecologia 73, 621–625.CrossRefGoogle Scholar
Rivero-Lynch, AP and Godfray, HCJ (1997) The dynamics of egg production, oviposition and resorption in a parasitoid wasp. Functional Ecology 11, 184–188.CrossRefGoogle Scholar
Roitberg, BD and Mangel, M (1988) On the evolutionary ecology of marking pheromones. Evolutionary Ecology 2, 289–315.CrossRefGoogle Scholar
SAS Institute (2007) JMP Statistical Discovery Software, version 7.0.1. Cary, NC: SAS Institute Inc.Google Scholar
Schoener, TW (1983) Field experiments on interspecific competition. The American Naturalist 122, 240–285.CrossRefGoogle Scholar
Sivinski, J, Aluja, M and López, M (1997) Spatial and temporal distributions of parasitoids of Mexican Anastrepha species (Diptera: Tephritidae) within the canopies of fruit trees. Annals of the Entomological Society of America 90, 604–618.CrossRefGoogle Scholar
Sivinski, J, Piñero, J and Aluja, M (2000) The distribution of parasitoids (Hymenoptera) of Anastrepha fruit flies (Diptera: Tephritidae) along an altitudinal gradient in Veracruz, Mexico. Biological Control 18, 258–269.CrossRefGoogle Scholar
Smith, SM (1996) Biological control with Trichogramma: advances, successes, and potential of their use. Annual Review of Entomology 41, 375–406.CrossRefGoogle ScholarPubMed
Statgraphics (2008) Statgraphics Centurion XV User Manual. Herndon, VA: Statgraphics.Google Scholar
Stephens, DW and Krebs, JR (1986) Foraging Theory. Princeton, NJ: Princeton University Press.Google Scholar
Ueno, T (1994) Self-recognition by the parasitic wasp Itoplectis naranyae (Hymenoptera: Ichneumonidae). Oikos 70, 333–339.CrossRefGoogle Scholar
van Alphen, JJ and Visser, ME (1990) Superparasitism as an adaptive strategy for parasitoids. Annual Review of Entomology 35, 59–79.CrossRefGoogle ScholarPubMed
van Baaren, J, Landry, BL and Boivin, G (1999) Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio. Functional Ecology 13, 66–71.CrossRefGoogle Scholar
van Dijken, MJ and Waage, JK (1987) Self and conspecific superparasitism by the egg parasitoid Trichogramma evanescens. Entomologia Experimentalis et Applicata 43, 183–192.CrossRefGoogle Scholar
van Lenteren, JC (1981) Host discrimination by parasitoids. In Nordlund, AD, Jones, RL and Lewis, WL (eds), Semiochemicals: Their Role in Pest Control. New York: John Wiley and Sons, pp. 153–179.Google Scholar
Vet, LEM and Dicke, M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37, 141–172.CrossRefGoogle Scholar
Vinson, SB (1976) Host selection by insect parasitoids. Annual Review of Entomology 21, 109–133.CrossRefGoogle Scholar
Vinson, SB and Ables, JR (1980) Interspecific competition among endoparasitoids of tobacco budworm larvae (Lep.: Noctuidae). Entomophaga 25, 357–362.CrossRefGoogle Scholar
Vinson, SB and Iwantsch, GF (1980) Host regulation by insect parasitoids. The Quarterly Review of Biology 55, 143–165.CrossRefGoogle Scholar
Visser, ME, Luyckx, B, Nell, HW and Boskamp, GJF (1992) Adaptive superparasitism in solitary parasitoids: marking of parasitized hosts in relation to the pay-off from superparasitism. Ecological Entomology 17, 76–82.CrossRefGoogle Scholar
Waage, JK, Carl, KP, Mills, NJ and Greathead, DJ (1985) Rearing entomophagous insects. In Singh, P and Moore, RF (eds), Handbook of Insect Rearing, vol. 1. Amsterdam: Elsevier, pp. 45–46.Google Scholar
Wang, XY, Yang, ZQ, Wu, H and Gould, JR (2008) Effects of host size on the sex ratio, clutch size, and size of adult Spathius agrili, an ectoparasitoid of emerald ash borer. Biological Control 44, 7–12.CrossRefGoogle Scholar