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Comparison of the Host Searching and Oviposition Behaviors of the Tephritid (Diptera) Parasitoids Aganaspis pelleranoi and Odontosema anastrephae (Hymenoptera: Figitidae, Eucoilinae)

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Abstract

We compared the host-searching and oviposition behaviors of two Neotropical figitid parasitoids (Hymenoptera) that exploit the same resource: ripe fruit infested by fruit fly larvae (Tephritidae) that have fallen to the ground. Sexually mature Aganaspis pelleranoi (Brèthes) and Odontosema anastrephae Borgmeier females were exposed individually, under no choice conditions, to four types of fruit: 1) Clean, intact guavas, Psidium guajava L. (no fruit fly larvae, no perforations); 2) clean, with artificial perforations; 3) artificially infested (with larvae), no perforations; 4) infested with artificial perforations. A behavioral transition matrix and sequence diagram of the following behaviors was constructed: walking on fruit, detection of larvae via the antennae, tarsi or aculeus, fruit perforation and penetration, and oviposition. Overall, we found that infested fruit (intact and with artificial perforations) elicited the most activity in the females of both species and that A. pelleranoi females exhibited a significantly more diverse behavioral repertoire (i.e., more transitions) and were significantly more active than O. anastrephae females. Females of both species penetrated the fruit in search of larvae by biting through the epi- and mesocarp, but O. anastrephae remained inside for significantly longer periods (up to eight hours). A. pelleranoi females used both their antennae and tarsi to detect larvae but the use of these structures varied depending on context: in infested fruit tarsi were used preferentially (usually while standing still) while in uninfested fruit, antennae were mainly used (usually while walking). In the case of O. anastrephae females the reverse pattern was usually observed with antennae most commonly used to detect larvae in infested fruit. We discuss our findings in light of their evolutionary, ecological and practical implications.

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References

  • Aluja M, López M, Sivinski J (1998) Ecological evidence for diapause in four native and one exotic species of larval-pupal fruit fly (Diptera: Tephritidae) parasitoids in tropical environments. Ann Entomol Soc Am 91:821–833

    Google Scholar 

  • Aluja M, Sivinski J, Ovruski S, Guillén L, Cancino J, López M, Torres-Anaya A, Gallegos-Chan G, Ruíz L (2009). Colonization and domestication of seven species of native new world hymenopterous larval-pupal and pupal fruit fly (Diptera: Tephritidae) parasitoids. Biocontrol Sci Techn doi: 10.1080/09583150802377373

  • Bernstein C, Driessen G (1996) Patch-marking and optimal search patterns in the parasitoid Venturia canescens. J Anim Ecol 65:211–219

    Article  Google Scholar 

  • Broad G, Quike D (2000) The adaptive significance of host location by vibrational sounding in parasitoid wasps. Proc R Soc London B 267:2403–2409

    Article  CAS  Google Scholar 

  • Buffington ML (2007) The occurrence and phylogenetic implications of the ovipositor clip within Figitidae (Insecta: Hymenoptera: Cynipoidea). J Nat Hist 41:33–36

    Article  Google Scholar 

  • Canale A, Raspi A (2000) Host location and oviposition behaviour in Opius concolor Szépligeti (Hymenoptera, Braconidae). Entomol Problems 31:25–32

    Google Scholar 

  • Conover WJ, Iman RL (1981) Rank transformation as a bridge between parametric and nonparametric statistics. Amer Statist 35:124–129

    Article  Google Scholar 

  • Doutt RL (1959) The biology of parasitic Hymenoptera. Annu Rev Entomol 4:161–182

    Article  Google Scholar 

  • Eben A, Benrey B, Sivinski J, Aluja M (2000) Host species and host plant effects on performance of Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environ Entomol 29:87–94

    Article  Google Scholar 

  • Eitam A, Holler T, Sivinski J, Aluja M (2003) Use of host fruit chemical cues for laboratory rearing of Doryctobracon areolatus (Hymenoptera: Braconidae), a parasitoid of Anastrepha spp. (Diptera: Tephritidae). Fla Entomol 86:211–216

    Article  Google Scholar 

  • Eskafi FM (1990) Parasitism of fruit flies Ceratitis capitata and Anastrepha (Diptera: Tephritidae) in Guatemala. Entomophaga 35:355–362

    Article  Google Scholar 

  • Faeth S (1990) Structural damage to oak leaves alters natural enemy attack on a leafminer. Ent Exp Appl 57:57–63

    Article  Google Scholar 

  • Fontal-Cazalla FM, Buffington ML, Nordlander G, Liljeblad J, Ros-Farré P, Nieves- Aldrey JL, Pujade-Villar J, Ronquist F (2002) Phylogeny of the Eucoilinae (Hymenoptera: Cynipoidea: Figitidae). Cladistics 18:154–199

    Article  Google Scholar 

  • Gallegos-Chan GJ (1999) Edad Óptima de Parasitación, Longevidad, Fecundidad y Patrones Diarios de Oviposición de 6 Especies de Parasitoides Nativos y 2 Exóticos de las Moscas de la Fruta del Género Anastrepha (Schiner) (Diptera: Tephritidae). BSc Thesis, Universidad Veracruzana. Xalapa, Veracruz, México, p 69

    Google Scholar 

  • García-Medel D, Sivinski J, Díaz-Fleischer F, Ramírez-Romero R, 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. Biol Control 43:12–22

    Article  Google Scholar 

  • Glas PC, Vet MEM (1983) Host-habitat location and host location by Diachasma alloeum muesebeck (Hym.: Braconidae) a parasitoid of Rhagoletis pomonella Walsh (Dipt.:Tephritidae). Neth J Zool 33:41–54

    Article  Google Scholar 

  • Godfray HCJ (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Greany PD, Tumlinson JH, Chambers DL, Boush GM (1977) Chemically mediated host finding by Biosteres (Opius) longicaudatus, a parasitoid of Tephritid fruit fly larvae. J Chem Ecol 3:189–195

    Article  CAS  Google Scholar 

  • Guimarães JA, Zucchi RA (2004) Parasitism behavior of three species of Eucolinae (Hymenoptera: Figitidae) fruit fly parasitoids (Diptera) in Brazil. Neotrop Entomol 33:217–224

    Article  Google Scholar 

  • Guimarães JA, Zucchi RA, Díaz NB, de Souza FMF, Uchoa FMA (1999) Species of Eucoilinae (Hymenoptera: Cynipoidea: Figitidae) parasitoids of frugivorous larvae (Diptera: Tephritidae and Lonchaeidae) in Brazil. Anais Soc Entomol Brasil 28:263–273

    Google Scholar 

  • Guimarães JA, Diaz NB, Zucchi RA (2000) Parasitoides—Figitidae (Eucoilinae). In: Malavasi A, Zucchi RA (eds) Moscas-das-frutas de Importância Econômica no Brasil. Conhecimento básico e aplicado, Holos Editora Ltda-Me, Riberão Preto, Brasil, pp 127–134

    Google Scholar 

  • Guimarães JA, Gallardo FE, Diaz NB, Zucchi RA (2003) Eucoilinae species (Hymenoptera: Cynipoidea: Figitidae) parasitoids of fruit-infesting dipterous larvae in Brazil: identity, geographical distribution and host associations. Zootaxa 278:1–23

    Google Scholar 

  • Guimarães JA, de Souza MF, Raga A, Zucchi RA (2004) Levantamento e interações tritróficas de figítidos (Hymenoptera: Eucoilinae) parasitóides de larvas frugívoras (Diptera) no Brasil. Arq Int Biol Sao Paulo 71:51–56

    Google Scholar 

  • Guimarães JA, Gallardo FE, Diaz NB (2005) Contribution to the systematic of Odontosema Kieffer (Hymenoptera: Cynipoidea, Figitidae). Trans Am Ent Soc 131:457–461

    Google Scholar 

  • Hassel MP, Southwood TRE (1978) Foraging strategies of insects. Annu Rev Ecol & Syst 9:75–98

    Article  Google Scholar 

  • Hoffmeister TS, Gienapp P (1999) Exploitation of the host’s chemical communication in a parasitoid searching for concealed host larvae. Ethology 105:223–232

    Article  Google Scholar 

  • Isidoro N, Bin F, Colazza S, Vinson SB (1996) Morphology of antennal gustatory sensilla and glands in some parasitoid Hymenoptera with hypothesis on their role in sex and host recognition. J Hym Res 5:206–239

    Google Scholar 

  • Kramer M, Schmidhammer J (1992) The chi-squared statistic in ethology: use and misuse. Anim Behav 44:833–841

    Article  Google Scholar 

  • Lawrence P (1981) Host vibration- a cue to host location by the parasite, Biosteres longicaudatus. Oecologia 48:249–251

    Article  Google Scholar 

  • Lehner PN (1996) Handbook of Ethological Methods. Cambridge Univ, Press, Cambridge, UK

    Google Scholar 

  • Leyva JL, Browning HW, Gilstrap FE (1991) Effect of host fruit species, size, and color on parasitization of Anastrepha ludens (Diptera: Tephritidae) by Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environ Entomol 20:1470–1474

    Google Scholar 

  • López M, Aluja M, Sivinski J (1999) Hymenopterous larval-pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in Mexico. Biol. Control 15:119–129

    Article  Google Scholar 

  • Matrangolo WJR, Nascimento AS, Carvalho RS, Melo ED, de Jesus M (1998) Fruit fly parasitoids associated with tropical fruits. Anais Soc Ent Brasil 27:593–603

    Google Scholar 

  • Mattiacci L, Hütter E, Dorn S (1999) Host location of Hyssopus pallidus, a larval parasitoid of the Codling moth. Cydia pomonella Biol Control 15:241–251

    Article  Google Scholar 

  • Messing RH, Jang EB (1992) Response of the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to host fruit stimuli. Environ Entomol 21:1189–1195

    Google Scholar 

  • Messing RH, Wong TTY (1992) An effective trapping method for field studies of Opiine braconid parasitoids of Tephritid fruit flies. Entomophaga 37:391–396

    Article  Google Scholar 

  • Messing RH, Klungness LM, Jang EB, Nishida KA (1996) Response of the melon fly parasitoid Psyttalia fletcheri (Hymenoptera: Braconidae) to host-habitat stimuli. J Insect Behav 9:933–945

    Article  Google Scholar 

  • Meyhöfer R, Casas J (1999) Vibratory stimuli in host location by parasitic wasps. J Ins Physiol 45:967–971

    Article  Google Scholar 

  • Meyhofer R, Casas J, Dorn S (1994) Host location by a parasitoid using leafminer vibrations: Characterizing the vibrational signals produced by the leafmining host. Physiol Entomol 19:349–459

    Article  Google Scholar 

  • Ngi-Song AJ, Overholt WA, Njagi PGN, Dicke M, Ayertey JN, Lande W (1996) Volatile infochemicals used in host and host habitat location by Cotesia flavipes Cameron and Cotesia sesamiae (Cameron) (Hymenoptera: Braconidae), larval parasitoids of stemborers on graminae. J Chem Ecol 22:307–323

    Article  CAS  Google Scholar 

  • Nishida T, Napompeth B (1974) Trap for tephritid fruit fly parasites. Entomophaga 19:349–351

    Article  Google Scholar 

  • Ovruski SM (1994a) Comportamiento en la detección del huésped en Aganaspis pelleranoi (Brèthes) (Hymenoptera: Cynipoidea, Eucoilidae) parasitoide de larvas de Ceratitis capitata (Wied.) (Diptera: Tephritidae). Rev Soc Entomol Argent 53:121–127

    Google Scholar 

  • Ovruski SM (1994b) Immature stages of Aganaspis pelleranoi (Brèthes) (Hymenoptera: Cynipoidea, Eucoilidae), a parasitoid of Ceratitis capitata (Wied.) and Anastrepha spp. (Diptera: Tephritidae). J Hym Res 3:233–239

    Google Scholar 

  • Ovruski SM (1995) Pupal and larval-pupal parasitoids (Hymenoptera) obtained from Anastrepha spp. and Ceratitis (Diptera: Tephritidae) pupae collected in four localities of Tucumán, Province, Argentina. Entomophaga 40:367–370

    Article  Google Scholar 

  • Ovruski SM, Aluja M, Sivinski J, 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. Int Pest Manag Rev 5:81–107

    Article  Google Scholar 

  • Ovruski SM, Schliserman P, Aluja M (2004) Indigenous parasitoids (Hymenoptera) attacking Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in native and exotic host plants in Northwestern Argentina. Biol Control 29:43–57

    Article  Google Scholar 

  • Ovruski SM, Wharton RA, Schliserman P, Aluja M (2005) Abundance of Anastrepha fraterculus (Diptera: Tephritidae) and its associated native parasitoids (Hymenoptera) in “feral” guavas growing in the endangered northernmost Yungas forest of Argentina with an update on the taxonomic status of opiine parasitoids previously reported in this country. Environ Entomol 34:807–818

    Google Scholar 

  • Piedra E, Zuñiga A, Aluja M (1993) New host plant and parasitoid record in México for Anastrepha alveata Stone (Diptera: Tephritidae). Proc Entomol Soc Wash 95:127

    Google Scholar 

  • Potting R, Vet L, Dicke M (1995) Host microhabitat location by the stemborer parasitoid Cotesia flavipes: the role of herbivore volatiles and locally and systematically induced plant volatiles. J Chem Ecol 21:525–539

    Article  CAS  Google Scholar 

  • Reitz S, Trumble J (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47:435–465

    Article  PubMed  CAS  Google Scholar 

  • Richerson J, Borden J (1972) Host finding by heat perception in Coeloides brunneri (Hymenoptera: Braconidae). Can Entomol 104:1877–1881

    Google Scholar 

  • Silvestri F (1913) Viaggio in Africa per cercare parassiti di mosche dei frutti. Boll Lab Zool Gen Agr Portici 8:1–164

    Google Scholar 

  • Sivinski J, Aluja M, López M (1997) The spatial and temporal distributions of parasitoids of Mexican Anastrepha species (Diptera: Tephritidae) within the canopies of fruit trees. Ann Entomol Soc Am 90:604–618

    Google Scholar 

  • Sivinski J, Piñero J, Aluja M (2000) The distributions of parasitoids (Hymenoptera) of Anastrepha fruit flies (Diptera: Tephritidae) along an altitudinal gradient in Veracruz, Mexico. Biol Control 18:258–269

    Article  Google Scholar 

  • Sivinski J, Vulinec K, Aluja M (2001) Ovipositor length in a guild of parasitoids (Hymenoptera: Braconidae) attacking Anastrepha spp. fruit flies (Diptera: Tephritidae) in southern Mexico. Ann Entomol Soc Am 94:886–895

    Article  Google Scholar 

  • Slater PJB, Ollason JC (1972) The temporal pattern of behavior in isolated male zebra finches: Transition analysis. Behaviour 42:248–269

    Article  Google Scholar 

  • Sokolowski MB, Turlins TCJ (1987) Drosophila parasitoid-host interaction: vibrotaxis and ovipositor searching from the host perspective. Can J Zool 65:461–464

    Article  Google Scholar 

  • Stat-Soft (1995) Statistica: User Guides. Stat-Soft, Inc, Tulsa, OK, USA

    Google Scholar 

  • Steimberg S, Dicke M, Vet LEM, Wanningen R (1992) Response of the braconid parasitoid Cotesia (= Apanteles) glomerata to volatile infochemicals: effect of bioassay set-up, parasitoid age and experience and barometrix flux. Exp Appl 63:163–175

    Article  Google Scholar 

  • Tumlinson JH, Turlings TCJ, Lewis WJ (1993) Semiochemically mediated foraging behaviour in beneficial parasitic insects. Arch Insect Bioch Physiol 22:385–391

    Article  CAS  Google Scholar 

  • Turica A (1968) Lucha biológica como medio de control de las moscas de los frutos. Revista IDIA 241:29–38

    Google Scholar 

  • van Alphen JJM, Drijver RAB (1982) Host selection by Asobara tabida Ness (Braconidae: Alysiinae), a larval parasitoid of fruit-inhabiting Drosophila species I. Host stage selection with Drosophila melanogaster as host species. J Zool 32:194–214

    Google Scholar 

  • van Alphen JJM, Vet LEM (1986) An evolutionary approach to host finding and selection. In: Waage J, Greathead D (eds) Insect Parasitoids. Academic Press, FL, pp 23–61

    Google Scholar 

  • van Dijken MJ, Van Alphen JJM (1998) The ecological significance of differences in host detection behavior in coexisting parasitoid species. Ecol Entomol 23:265–270

    Article  Google Scholar 

  • van Lenteren JC, Isidoro N, Bin F (1998) Functional anatomy of the ovipositor clip in the parasitoid Leptopilina heterotoma (Thompson) (Hymenoptera: Eucoilidae), a structure to grip escaping larvae. Int J Insect Morphol Embryol 27:263–268

    Article  Google Scholar 

  • Vet LEM, Bakker K (1985) A comparative functional approach to the host detection behaviour of parasitic wasps. 2. A quantitative study on eight eucoilid species. Oikos 44:487–498

    Article  Google Scholar 

  • Vet L, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Ann Rev Entomol 37:141–172

    Article  Google Scholar 

  • Vet LEM, van Alphen JJM (1985) A comparative functional approach to the host detection behaviour of parasitic wasps. 1. A qualitative study on Eucolidae and Alysiinae. Oikos 44:478–486

    Article  Google Scholar 

  • Vet LEM, Wäckers FL, Dicke M (1992) How to hunt for hiding hosts: the reliability-detectability problem in foraging parasitoids. Neth J Zool 41:202–213

    Article  Google Scholar 

  • Vinson SB (1976) Host selection by insect parasitoids. Ann Rev Entomol 21:109–134

    Article  Google Scholar 

  • Vinson SB (1984) Parasitoid-host relationships. In: Bell WJ, Cardé RJ (eds) The Chemical Ecology of Insects. Chapman and Hall, NY, USA, pp 205–233

    Google Scholar 

  • Vinson SB (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–96

    Article  Google Scholar 

  • Webb JC, Landolt PJ (1984) Detecting insect larvae in fruit by vibrations produced. J Environ Sci Health, Part A Environ. Sci Eng 19:367–375

    Google Scholar 

  • Weseloh RM (1981) Host location by parasitoids. In: Nordlund DA, Jones RL, Lewis WJ (eds) Semiochemicals: Their role in pest control. John Wiley & Sons, New York, USA, pp 79–95

    Google Scholar 

  • Wharton RA, Gilstrap FE, Rhode RH, Fischel MM, Hart WG (1981) Hymenopterous egg-pupal and larval-pupal parasitoids of Ceratitis capitata and Anastrepha spp. (Diptera: Tephritidae) in Costa Rica. Entomophaga 26:285–290

    Article  Google Scholar 

  • Wharton RA, Ovruski SM, Gilstrap FE (1998) Neotropical Eucoilidae (Cynipoidea) associated with fruit infesting Tephritidae, with new records from Argentina, Bolivia and Costa Rica. J Hym Res 7:102–115

    Google Scholar 

  • Yépes RF, Vélez R (1989) Contribución al conocimiento de las moscas de la fruta (Tephritidae) y sus parasitoides en el Departamento de Antioquia. Rev Fac Agron Medellín 42:73–98

    Google Scholar 

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Acknowledgements

We gratefully acknowledge the expert advice provided by Marissa Mora Acosta (Instituto de Ecología, A.C.) while running sequence and statistical analyses. We also thank Alberto Anzures-Dadda for his all-encompassing support during manuscript preparation. Main financial support for this study was furnished by the Mexican Campaña Nacional contra las Moscas de la Fruta (Secretaría de Agricultura, Ganadería, Desarrollo Rural y Pesca - Instituto Interamericano de Cooperación para la Agricultura (SAGARPA-IICA), the Consejo Nacional de Ciencia y Tecnología (Project CONACyT—SEP-2004-C01-46846) and the United Status Department of Agriculture (Agricultural Research Service). S.M. Ovruski and L.E. Oroño also acknowledge financial support from the Consejo Nacional de Investigaciones Científicas y Técnicas de la República Argentina (CONICET) (grants PIP No. 02567/01, and No. 5129/05). S.M. Ovruski acknowledges a fellowship by the International Atomic Energy Agency (IAEA) that allowed him to visit the Instituto de Ecología, A.C. and collaborate on this study. Finally, M. Aluja also acknowledges support from CONACyT through a Sabbatical Year Fellowship (Ref. 79449) and thanks Benno Graf and Jörg Samietz (Forschungsanstalt Agroscope Changins-Wädenswil ACW), for providing ideal working conditions to finish writing/revising this paper.

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  1. Instituto de Ecología, A.C., Apartado Postal 63, 91000, Xalapa, Veracruz, México

    Martín Aluja & Larissa Guillén

  2. PROIMI Biotecnología—CONICET, División Control Biológico de Plagas, Av. Belgrano y Pje. Caseros S/N, T4001MVB—San Miguel de Tucumán, Tucumán, Argentina

    Sergio M. Ovruski & Luis E. Oroño

  3. Center for Medical, Agricultural & Veterinary Entomology, USDA-ARS, 1600/1700 SW 23rd Drive, Gainesville, FL, 32608, USA

    John Sivinski

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  1. Martín Aluja
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Aluja, M., Ovruski, S.M., Guillén, L. et al. Comparison of the Host Searching and Oviposition Behaviors of the Tephritid (Diptera) Parasitoids Aganaspis pelleranoi and Odontosema anastrephae (Hymenoptera: Figitidae, Eucoilinae). J Insect Behav 22, 423–451 (2009). https://doi.org/10.1007/s10905-009-9182-3

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