Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-31T13:33:59.810Z Has data issue: false hasContentIssue false
  • English
  • Français

Host discrimination in the fruit fly parasitoid Diachasmimorpha longicaudata: evidence from virgin female behaviour and egg distribution patterns

Published online by Cambridge University Press:  18 September 2020

Francisco Devescovi ,
Guillermo E. Bachmann ,
Ana L. Nussenbaum ,
Mariana M. Viscarret ,
Jorge L. Cladera  and
Diego F. Segura Open the ORCID record for Diego F. Segura [Opens in a new window]
Francisco Devescovi
Affiliation:
Laboratorio de Insectos de Importancia Agronómica, IGEAF (INTA), GV-IABIMO (CONICET), Dr Nicolás Repetto y De los Reseros s/n, Hurlingham (B1686IGC), Buenos Aires, Argentina
Guillermo E. Bachmann
Affiliation:
Laboratorio de Insectos de Importancia Agronómica, IGEAF (INTA), GV-IABIMO (CONICET), Dr Nicolás Repetto y De los Reseros s/n, Hurlingham (B1686IGC), Buenos Aires, Argentina
Ana L. Nussenbaum
Affiliation:
Laboratorio de Insectos de Importancia Agronómica, IGEAF (INTA), GV-IABIMO (CONICET), Dr Nicolás Repetto y De los Reseros s/n, Hurlingham (B1686IGC), Buenos Aires, Argentina
Mariana M. Viscarret
Affiliation:
Insectario de Investigaciones para Lucha Biológica, IMyZA (INTA), GV-IABIMO (CONICET), Dr Nicolás Repetto y De los Reseros s/n, Hurlingham (B1686IGC), Buenos Aires, Argentina
Jorge L. Cladera
Affiliation:
Laboratorio de Insectos de Importancia Agronómica, IGEAF (INTA), GV-IABIMO (CONICET), Dr Nicolás Repetto y De los Reseros s/n, Hurlingham (B1686IGC), Buenos Aires, Argentina
Diego F. Segura*
Affiliation:
Laboratorio de Insectos de Importancia Agronómica, IGEAF (INTA), GV-IABIMO (CONICET), Dr Nicolás Repetto y De los Reseros s/n, Hurlingham (B1686IGC), Buenos Aires, Argentina
*
Author for correspondence: Diego F. Segura, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Many parasitoid species discriminate already parasitized hosts, thus avoiding larval competition. However, females incur in superparasitism under certain circumstances. Superparasitism is commonly observed in the artificial rearing of the parasitoid Diachasmimorpha longicaudata, yet host discrimination has been previously suggested in this species. Here, we addressed host discrimination in virgin D. longicaudata females in a comprehensive way by means of direct and indirect methods, using Ceratitis capitata and Anastrepha fraterculus which are major fruit fly pests in South America. Direct methods relied on the description of the foraging behaviour of females in arenas with parasitized and non-parasitized host larvae. In the indirect methods, healthy larvae were offered to single females and the egg distributions were compared to a random distribution. We found that D. longicaudata was able to recognize parasitized host from both host species, taking 24 h since a first parasitization for A. fraterculus and 48 h for C. capitata. Indirect methods showed females with different behaviours for both host species: complete discrimination, non-random (with superparasitism), and random distributions. A larger percentage of females reared and tested on A. fraterculus incurred in superparasitism, probably associated with higher fecundity. In sum, we found strong evidence of host discrimination in D. longicaudata, detecting behavioural variability associated with the host species, the time since the first parasitization and the fecundity of the females.

Keywords

Avoidance of superparasitismBraconidaeDipteraegg distribution patternshost choicehymenopteraparasitoid foraging behaviourTephritidae
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 2 , April 2021 , pp. 229 - 237
Check for updates
Copyright
Copyright © The Author(s), 2020. 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.)

References

Altafini, DL, Redaelli, LR and Jahnke, SM (2013) Superparasitism of Ceratitis capitata and Anastrepha fraterculus (Diptera: Tephritidae) by Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Florida Entomologist 96, 391–395.CrossRefGoogle Scholar
Amat, I, Desouhant, E and Bernstein, C (2009) Differential use of conspecific-derived information by sexual and asexual parasitic wasps exploiting partially depleted host patches. Behavioral Ecology and Sociobiology 63, 563–572.CrossRefGoogle Scholar
Anderson, P (1988) Äggläggningshämmande feromoner hos insekter. Entomologisk Tidskrift 109, 14–18.Google Scholar
Ardeh, MJ, de Jong, PW and van Lenteren, JC (2005) Intra- and interspecific host discrimination in arrhenotokous and thelytokous Eretmocerus spp. Biological Control 33, 74–80.CrossRefGoogle Scholar
Bai, B and Mackauer, M (1990) Host discrimination by the aphid parasitoid Aphelinus asychis (Hymenoptera: Aphelinidae): when superparasitism is not adaptive. The Canadian Entomologist 122, 363–372.CrossRefGoogle Scholar
Bai, B and Mackauer, M (1992) Influence of superparasitism on development rate and adult size in a solitary parasitoid Aphidius ervi. Functional Ecologist 6, 302–307.CrossRefGoogle Scholar
Bakker, KJJM, 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
Bakker, K, Peulet, PH and Visser, ME (1990) The ability to distinguish between hosts containing different numbers of parasitoid eggs by the solitary parasitoid Leptopilina heterotoma (Thomson) (Hym. Cynip.). Netherlands Journal of Zoology 40, 514–520.CrossRefGoogle Scholar
Bernstein, C and Jervis, M (2008) Food-searching in parasitoids: the dilemma of choosing between ‘immediate’ or future fitness gains. In Wajnberg, E, Bernstein, C and van Alphen, JJM (eds), Behavioural Ecology of Insect Parasitoids-From Theoretical Approaches to Field Applications. Oxford, UK: Blackwell Publishing Ltd, pp. 129–171.CrossRefGoogle Scholar
Brodeur, J and Boivin, G (2004) Functional ecology of immature parasitoids. Annual Review of Entomology 49, 27–49.CrossRefGoogle ScholarPubMed
Cancino, J, Villalobos, P and De La Torre, S (2002) Changes in the rearing process to improve the quality of mass production of the fruit fly parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). In Leppla, NC, Bloem, KA and Luck, R (eds), Quality Control for Mass- Reared Arthropods. Proc. 8th and 9th workshop of the IOBC, University of Florida, Florida, USA, pp. 74–82.Google Scholar
Carbone, SS and Rivera, AC (2003) Egg load and adaptive superparasitism in Anaphes nitens, an egg parasitoid of the Eucalyptus snout-beetle Gonipterus scutellatus. Entomologia Experimentalis et Applicata 106, 127–134.CrossRefGoogle Scholar
Chau, NNB and Maeto, K (2008) Intraspecific larval competition in Meteorus pulchricornis (Hymenoptera: Braconidae), a solitary endoparasitoid of lepidopteran larvae. Applied Entomology and Zoology 43, 159–165.CrossRefGoogle Scholar
Chow, FJ and Mackauer, M (1986) Host discrimination and larval competition in the aphid parasite Ephedrus californicus. Entomologia Experimentalis et Applicata 41, 243–254.CrossRefGoogle Scholar
Danyk, TP and Mackauer, M (1993) Discrimination between self-and conspecific-parasitized hosts in the aphid parasitoid Praon pequodorum Viereck (Hymenoptera: Aphidiidae). The Canadian Entomologist 125, 957–964.CrossRefGoogle Scholar
Darrouzet, E, Bignon, L and Chevrier, C (2007) Impact of mating status on egg-laying and superparasitism behaviour in a parasitoid wasp. Entomologia Experimentalis et Applicata 123, 279–285.CrossRefGoogle Scholar
Devescovi, F, Bachmann, GE, Nussenbaum, AL, Viscarret, MM, Cladera, JL and Segura, DF (2017) Effects of superparasitism on immature and adult stages of Diachasmimorpha longicaudata Ashmead (Hymenoptera: Braconidae) reared on Ceratitis capitata Wiedemann (Diptera: Tephritidae). Bulletin of Entomological Research 107, 756–767.CrossRefGoogle Scholar
Fellowes, MDE, van Alphen, JJM and Jervis, MA (2005) Foraging behaviour. In Jervis, MA (ed.), Insects as Natural Enemies: A Practical Perspective. Dordrecht, The Netherlands: Springer, pp. 1–71.Google Scholar
Godfray, H.C.J. (1994) Parasitoids – Behavioural and Evolutionary Ecology, 1st Edn. New Jersey, USA: Princeton University Press, 473 p.CrossRefGoogle Scholar
González, PI, Montoya, P, Perez-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, Harvey, IF and Thompson, DJ (1993) The effect of superparasitism on development of the solitary parasitoid wasp, Venturia canescens (Hymenoptera: Ichneumonidae). Ecological Entomology 18, 203–208.CrossRefGoogle Scholar
Hemerik, L, van der Hoeven, N and van Alphen, JJM (2002) Egg distributions and the information a solitary parasitoid has and uses for its oviposition decisions. Acta Biotheoretica 50, 167–188.CrossRefGoogle ScholarPubMed
Hoffmeister, TS and Wajnberg, E (2008) Finding optimal behaviors with genetic algorithms. In Wajnberg, E, Bernstein, C and van Alphen, JJM (eds), Behavioural Ecology of Insect Parasitoids-From Theoretical Approaches to Field Applications. Oxford, UK: Blackwell Publishing Ltd, pp. 384–401.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
Jaldo, HE, Gramajo, MC and Willink, E (2001) Mass rearing of Anastrepha fraterculus (Diptera: Tephritidae): a preliminary strategy. Florida Entomologist 84, 716–718.CrossRefGoogle Scholar
Jaldo, HE, Willink, E and Liedo, P (2007) Demographic analysis of mass-reared Anastrepha fraterculus (Diptera: Tephritidae) in Tucumán, Argentina. Revista Industrial y Agrícola de Tucumán 84, 15–20.Google Scholar
Jordão-Paranhos, BA, Walder, JM and Papadopoulos, NT (2003) A simple method to study parasitism and field biology of the parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) on Ceratitis capitata (Diptera: Tephritidae). Biocontrol Science and Technology 13, 631–639.Google Scholar
Michaud, JP (1994) Differences in foraging behaviour between virgin and mated aphid parasitoids. (Hymenoptera: Aphidiidae). Canadian Journal of Zoology 72, 1597–1602.CrossRefGoogle Scholar
Montoya, P and Cancino, J (2004) Control biológico por aumento en moscas de la fruta (Diptera: Tephritidae). Folia Entomológica Mexicana 43, 257–270.Google 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
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, Great Britain: Intercept/VHC Publishers, pp. 41–62.Google Scholar
Mangel, M (1987) Opposition site selection and clutch size in insects. Journal of Mathematical Biology 25, 1–22.CrossRefGoogle Scholar
McDonald, JH (2014) Student's t-test for two samples. In McDonald, JH (ed.), Handbook of Biological Statistics. 3rd Edn. Baltimore, Maryland, USA: Sparky House Publishing, pp. 127–131.Google Scholar
Meelis, E (1982) Egg distribution of insect parasitoids: a survey of models. Acta Biotheoretica 31, 109–126.CrossRefGoogle Scholar
Meirelles, RN, Redaelli, LR and Ourique, 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
Minkenberg, OP, Tatar, M and Rosenheim, JA (1992) Egg load as a major source of variability in insect foraging and oviposition behavior. Oikos 65, 134–142.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 and Technology 13, 683–690.CrossRefGoogle Scholar
Ovruski, SM, 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 Entomológica Argentina 62, 49–59.Google Scholar
Rogers, D (1975) A model for avoidance of superparasitism by solitary insect parasitoids. Journal of Animal Ecology 44, 623–638.CrossRefGoogle Scholar
Roitberg, BD, Sircom, J, Roitberg, CA, van Alphen, JJM and Mangel, M (1993) Life expectancy and reproduction. Nature 364, 108–108.CrossRefGoogle ScholarPubMed
Rosenheim, JA and Rosen, D (1991) Foraging and oviposition decisions in the parasitoid Aphytis lingnanensis: distinguishing the influences of egg load and experience. Journal of Animal Ecology 60, 873–893.CrossRefGoogle Scholar
Ruschioni, S, van Loon, JJ, Smid, HM and van Lenteren, JC (2015) Insects can count: sensory basis of host discrimination in parasitoid wasps revealed. PLoS ONE 10), e0138045.CrossRefGoogle ScholarPubMed
Rusina, LY (2011) Host discrimination by Elasmus schmitti (Hymenoptera, Eulophidae) and Latibulus argiolus (Hymenoptera, Ichneumonidae), parasitoids of colonies of Polistes wasps (Hymenoptera, Vespidae). Entomological Review 91, 1081–1087.CrossRefGoogle Scholar
Salles, LAB (1995) Bioecologia e controle da mosca-das-frutas sul-americana EMBRAPA-CPACT, Pelotas RS, Brazil, 58 p.Google Scholar
Salt, G (1961) Competition among insect parasitoids. In Salt, G (ed.), Mechanisms in Biological Competition, Vol. 15. Symposia of the Society for Experimental Biology. Cambridge, UK, pp. 96–119.Google Scholar
Segura, DF, Nussenbaum, AL, Viscarret, MM, Devescovi, F, Bachmann, GE, Corley, JC, Ovruski, SM and Cladera, JL (2016) Innate host habitat preference in the parasitoid Diachasmimorpha longicaudata: functional significance and modifications through learning. PLoS ONE 11, e0152222.CrossRefGoogle ScholarPubMed
Sirot, E and Bernstein, C (1996) Time sharing between host searching and food searching in parasitoids: state-dependent optimal strategies. Behavioral Ecology 7, 189–194.CrossRefGoogle Scholar
Sirot, E, Ploye, H and Bernstein, C (1997) State dependent superparasitism in a solitary parasitoid: egg load and survival. Behavioral Ecology 8, 226–232.CrossRefGoogle Scholar
Sousa, JM and Spence, JR (2000) Effects of mating status and parasitoid density on superparasitism and offspring fitness in Tiphodytes gerriphagus (Hymenoptera: Scelionidae). Annals of the Entomological Society of America 93, 548–553.CrossRefGoogle Scholar
Suárez, L, Buonocore Biancheri, MJ, Sánchez, G, Cancino, J, Murúa, F, Bilbao, M, Molina, D, Laria, O, Ovruski, SM (2020) Radiation on medfly larvae of tsl Vienna-8 genetic sexing strain displays reduced parasitoid encapsulation in mass-reared Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Journal of Economic Entomology 113, 1134–1144.CrossRefGoogle Scholar
Terán, HR (1977) Comportamiento alimentario y su correlación a la reproducción en hembras de Ceratitis capitata (Wied.) (Diptera, Trypetidae). Revista Agronómica del Noroeste Argentino.Google Scholar
Tunca, H and Kilinçer, 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.Google Scholar
van Alphen, JJM and Nell, HW (1982) Superparasitism and host discrimination by Asobara tabida Nees (Braconidae: Alysiinae), a larval parasitoid of Drosophilidae. Netherlands Journal of Zoology 32, 232–260.CrossRefGoogle Scholar
van Alphen, JJM and Visser, ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology 35, 59–79.CrossRefGoogle ScholarPubMed
van Alphen, JJM, van Dijken, MJ and Waage, JK (1987) A functional approach to superparasitism: host discrimination needs not to be learnt. Netherlands Journal of Zoology 37, 167–179.Google Scholar
van Alphen, JJM and Jervis, MA (1996) Foraging behavior: host discrimination. In Jervis, MA and Kidd, N (eds), Insect Natural Enemies. A Practical Approach to Their Study and Evaluation. Dordrecht, The Netherlands: Springer, pp. 32–36.Google 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 Dijken, MJ, van Stratum, P and van Alphen, JJM (1992) Recognition of individual-specific marked parasitized hosts by the solitary parasitoid Epidinocarsis lopezi. Behavioral Ecology and Sociobiology 30, 77–82.CrossRefGoogle Scholar
van Lenteren, JC (1981) Host discrimination by parasitoids. In van Lenteren, JC (ed.), Semiochemicals: Their Role in Pest Control. New York, USA: Wiley, pp. 153–179.Google Scholar
van Lenteren, JC, Bakker, K and van Alphen, JJM (1978) How to analyse host discrimination. Ecological Entomology 3, 71–75.CrossRefGoogle Scholar
Vera, T, Abraham, S, Oviedo, A and Willink, E (2007) Demographic and quality control parameters of Anastrepha fraterculus (Diptera: Tephritidae) maintained under artificial rearing. Florida Entomologist 90, 53–57.CrossRefGoogle Scholar
Viscarret, MM, La Rossa, R, Segura, DF, Ovruski, SM and Cladera, JL (2006) Evaluation of the parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) reared on a genetic sexing strain of Ceratitis capitata (Wied.) (Diptera: Tephritidae). Biological Control 36, 147–153.CrossRefGoogle Scholar
Visser, ME (1993) Adaptive self-and conspecific superparasitism in the solitary parasitoid Leptopilina heterotoma (Hymenoptera: Eucoilidae). Behavioral Ecology 4, 22–28.CrossRefGoogle Scholar
Visser, ME (1995) The effect of competition on oviposition decisions of Leptopilina heterotoma (Hymenoptera: Eucoilidae). Animal Behaviour 49, 1677–1687.CrossRefGoogle Scholar
Visser, ME, van Alphen, JJM and Nell, HW (1992) Adaptive superparasitism and patch time allocation in solitary parasitoids: the influence of pre-patch experience. Behavioral Ecology and Sociobiology 31, 163–171.CrossRefGoogle Scholar
Wajnberg, E (2009) Genetics of the behavioral ecology of egg parasitoids. In Consoli, F, Parra, J and Zucchi, R (eds), Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Progress in Biological Control, Vol. 9. Dordrecht, The Netherlands: Springer, pp. 149–165.CrossRefGoogle Scholar
Weisser, WW and Houston, AI (1993) Host discrimination in parasitic wasps: when is it advantageous? Functional Ecologist 7, 27–39.CrossRefGoogle Scholar
Wharton, RA (1989) Classical biological control of fruit-infesting Tephritidae. In Robinson, S and Hooper, G (eds), Fruit Flies: Their Biology, Natural Enemies and Control. Amsterdam, Holland: Elsevier, pp. 303–313.Google Scholar
Wharton, RA and Gilstrap, FE (1983) Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus S. l. (Diptera: Tephritidae). Annals of the Entomological Society of America 76, 721–742.CrossRefGoogle Scholar
Yamada, YY and Ikawa, K (2005) Superparasitism strategy in a semisolitary parasitoid with imperfect self/non-self recognition, Echthrodelphax fairchildii. Entomologia Experimentalis et Applicata 114, 143–152.CrossRefGoogle Scholar