Parasitoid-host interaction: sensory structures involved in the parasitism behavior of Bracon vulgaris (Hymenoptera: Braconidae)

in Animal Biology
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?

Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.


Have Institutional Access?

Access content through your institution. Any other coaching guidance?


Parasitoids have evolved mechanisms to evade their hosts’ defenses. Bracon vulgaris (Ashmead) is a larval ectoparasitoid responsible for natural reduction of Anthonomus grandis (Boheman) and Pectinophora gossypiella (Saunders), which are considered the main cotton pests in the cotton agro-ecosystem in northeastern Brazil. This study aimed to analyze the sensory structures (antennae and ovipositor) involved in the parasitism behavior of B. vulgaris, and to describe and evaluate associations between composition, morphology, and functions of these structures in the parasitoid-host interaction. Results showed that the B. vulgaris ovipositor is a multifunctional structure of 2.7 ± 0.3 mm in length composed of 3 valves. Valves 1 and 2 are elongated, rigid, and act jointly to pierce the host’s cuticle, to inject the poison glands secretion, and to deposit eggs. Valve 3 covers the other valves, giving them protection. Valve 3 also presents annulations in all its extension, which gives flexibility to the ovipositor, and trichoid sensilla that possibly capture vibrations from the host’s feeding and locomotion, thereby aiding the parasite in the host selection. The presence of cuticular microtrichia was possibly responsible for the cleaning of the ovipositor, keeping it functional between the various insertions that occur during the parasitism behavior. The parasitoid’s antennae are filliform-like, measure about 2 mm, and are composed of four types of sensilla (trichoids, basiconical, coeloconical, and placodes) that act as olfactory and gustatory receptors and/or express tactile, thermo,- and hygroreception functions. The integrated action of these sensory components corroborates the successful parasitism behavior of the parasitoid B. vulgaris.

Parasitoid-host interaction: sensory structures involved in the parasitism behavior of Bracon vulgaris (Hymenoptera: Braconidae)

in Animal Biology



AhmedT.ZhangT.HeK.BaiS.WangZ. (2013) Sense organs on the ovipositor of Macrocentrus cingulum Brischke (Hymenoptera: Braconidae); their probable role in stinging, oviposition and host selection process. J. Asia Pacific Entomol.16343-348.

AmalinD.M.PeñaJ.E.DucanR.E. (2005) Effects of host age, female parasitoid age, and host plant on parasitism of Ceratogramma etiennei (Hymenoptera: Trichogrammatidae). Fla. Entomol.8877-82.

AmornsakW.CribbB.GordhG. (1998) External morphology of antennal sensilla of Trichogramma Australicum Girault (Hymenoptera: Trichogrammatidae). Int. J. Insect Morphol. & Embryol.2767-82.

ArrekulB.Zaldivar-RiverónA.QuickeD.L.J. (2004) Venom gland and reservoir morphology of the genus Pseudoyelicones van Achterberg, Penteado-Dias & Quicke (Hymenoptera: Braconidae: Rogadinae) and implications for relationships. Zool. Med. Leiden78119-122.

BellowsT.S.FisherT.W. (1999) Handbook of Biological Control. 1st ed. Academic PressCalifornia.

BrownP.E.AndersonM. (1998) Morphology and ultrastructure of sense organs on the ovipositor of Trybliographa rapae, a parasitoid of the cabbage root fly. J. Insect Physiol.441017-1025.

ButterfieldA.AndersonM. (1994) Morphology and ultrastructure of antennal sensilla of the parasitoid, Trybliographa rapae (Westw.) (Hymenoptera: Cynipidae). Int. J. Insect Morphol. & Embryol.2311-20.

CanaleA.RaspiA. (2000) Host location and oviposition behaviour in Opius concolor (Hymenoptera: Braconidae). Ent. Prob.3125-32.

CarvalhoS.L.FernandesW.D.PatelP.N.HabibM.E.M. (2000a) Desenvolvimento de Bracon vulgaris Ashmead, ectoparasitóide de Pectinophora gossypiella Saunders, em laboratório. Braz. J. Ecol.1218-22.

CarvalhoS.L.FernandesW.D.PatelP.N.HabibM.E.M. (2000b) Respostas comparativas de Bracon vulgaris Ashmead (Hymenoptera: Braconidae) a diferentes macerados de plantas de algodão, em dois modos de exposição. Rev. Agric.7541-53.

CarvalhoS.L.FernandesW.D.HabibM.E.M.PatelP.N. (2002) Preferência de Bracon vulgaris e adequações de alguns hospedeiros em condições de laboratório. Rev. Agric.7739-56.

CeballoF.A.WalterG.H. (2004) Life history parameters and biocontrol potential of the mealybug parasitoid Coccidoxenoides peregrinus (Timberlake) (Hymenoptera: Encyrtidae): asexuality, fecundity and ovipositional patterns. Biolog. Control29235-244.

DweckH.K.M. (2009) Antennal sensory receptors of Pteromalus puparum female (Hymenoptera: Pteromalidae), a gregarious pupal endoparasitoid of Pieris rapae. Micron40769-774.

DweckH.K.M.GadallahN.S.DarwishE. (2008) Structure and sensory equipment of the ovipositor of Habrobracon hebetor (Say) (Hymenoptera: Braconidae). Micron391255-1261.

GaoY.LuoL.HammondA. (2007) Antennal morphology, structure and sensilla distribution in Microplitis pallidipes (Hymenoptera: Braconidae). Micron38684-693.

GoubaultM.CorteseroA.M.PatyC.FourrierJ.DourlotS.LeRalecA. (2011) Abdominal sensory equipment involved in external host discrimination in a solitary parasitoid wasp. Micros. Res. Tech.741145-1153.

GullanP.J.CranstonP.S. (2008) Os insetos: um resumo de entomologia. Terceira edição. Roca editoraSão Paulo.

GunduzE.A.GulelA. (2005) Investigation of fecundity and sex ratio in the parasitoid Bracon hebertor Say (Hymenoptera: Braconidae) in relation to parasitoid age. Turk. J. Zool.29291-294.

HaD.SongK.NhoS.LeeK. (2006) Host selection behaviors and progeny suitability of two parasitic wasps, Venturia canescens and Bracon hebertor, against abnormal host conditions of Plodia interpunctella. J. Asia Pacific Entomol.9353-360.

HajekA.E. (2004) Natural Enemies: An Introduction to Biological Control. 1st ed. Cambridge University PressCambridge.

HarbinsonJ.L.LegaspiJ.C.FabritiusS.L.SaldanaR.R.LegaspiB.C.Jr.EnkegaardA. (2001) Effects of age and host number on reproductive biology of Allorhogas pyralophagus (Hymenoptera: Braconidae) attacking the mexican rice Borer (Lepidoptera: Pyralidae). Environ. Entomol.30129-135.

HondaT.KainohY. (1998) Age-related fecundity and learning ability of the egg-larval parasitoid Ascogaster reticulatus Watanabe (Hymenoptera: Braconidae). Biolog. Control13177-181.

KlowdenM.J. (2007) Physiological Systems in Insects. 2nd ed. ElsevierLondon.

Le RalecA.RabasseJ.M.WajnbergE. (1996) Comparative morphology of the ovipositor of some parasitic Hymenoptera in relation to characteristics of their hosts. Can. Entomol.128413-433.

LiX.LuD.LiuX.ZhangQ.ZhouX. (2011) Ultrastructural characterization of olfactory sensilla and immunolocali-zation of odorant binding and chemosensory proteins from an ectoparasitoid Scleroderma guani (Hymenoptera: Bethylidae). Int. J. Biol. Sciences7848-868.

LiY.LuJ.KeX.FuW. (2007) Morphology and structure of the ovipositor in Macrocentrus cingulum (Hymenoptera: Braconidae), a polyembryonic parasitoid. J. Life Scienc.134-39.

MehrnejadM.R.CoplandM.J.W. (2006) Host-stage selection and oviposition behavior of Psyllaephagus pistaciae, parasitoid of the common pistachio psylla Agonoscena pistaciae. Biolog. Control36139-146.

MoreauS.J.M.VinchonS.CherquiA.PrévostG. (2009) Components of Asobara venoms and their effects on hosts. Adv. Insect Physiol.70217-232.

NénonJ.P.KacemN.LeLannicJ. (1997) Structure, sensory equipment, and secretions of the ovipositor in a giant species of Hymenoptera: Megarhyssa atrata F. (Ichneumonidae: Pimplinae). Can. Entomol.129789-799.

NortonW.N.VinsonS.B. (1974) Antennal sensila of three parasitic hymenoptera. Int. J. Insect Morphol. & Embryol.3305-316.

ObonyoM.SchulthessF.GeraldJ.WanyamaO.Le RuB.CalatayudP.A. (2008) Location, acceptance and suitability of lepidopteran stemborers feeding on a cultivated and wild host-plant to the endoparasitoid Cotesia flavipes Cameron (Hymenoptera: Braconidae). Biolog. Control4536-47.

OchiengS.A.ParkK.C.ZhuJ.W.BakerT.C. (2000) Functional morphology of antennal chemoreceptors of the parasitoid Microplitis croceipes (Hymenoptera: Braconidae). Arth. Struct. & Dev.29231-240.

OnagbolaE.O.FadamiroH.Y. (2008) Scanning electron microscopy studies of antennal sensilla of Pteromalus cerealellae (Hymenoptera: Pteromalidae). Micron39526-535.

PereiraF.P.ZanuncioJ.C.SerrãoJ.E.OliveiraH.O.FáveroK.GranceE.L.V. (2009) Progênie de Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae) parasitando pupas de Bombyx mori L. (Lepidoptera: Bombycidae) de diferentes idades. Neotrop. Entomol.38660-664.

PeydróR.J.GaríJ.V.F.MartosC.G.MaríJ.M. (1996) Comparative morphology of the venom apparatus in some subfamilias of braconid wasps (Hymenoptera: Braconidae). Bol. Asoc. Esp. Ent.20149-159.

PierozziI.Jr.HabibM.E.M. (1993) Aspectos biológicos e de comportamento dos principais parasitóides de Anthonomus grandis Boh. (Coleoptera: Curculionidae), em Campinas, SP. An. Soc. Entomol. Brasil22317-323.

PolidoriC.Nieves-AldreyJ.L. (2014) Diverse filters to sense: great variability of antennal morphology and sensillar equipment in gall-wasps (Hymenoptera: Cynipidae). Plos One91-26.

QuickeD.L.J. (1997) Parasitic Wasps. 1st ed. Chapman & HallCambridge.

RamalhoF.S.WanderleyP.A.MalaquiasJ.B.SouzaJ.V.S.RodriguesK.C.V.ZanuncioJ.C. (2009) Effect of temperature on the reproduction of Bracon vulgaris Ashmead (Hymenoptera: Braconidae), a parasitoid of the cotton boll weevil. Entomol. News120476-487.

Rukmowati-BrotodjojoR.R.WalterG.H. (2006) Oviposition and reproductive performance of a generalist parasitoid (Trichogramma pretiosum) exposed to host species that differ in their physical characteristics. Biolog. Control39300-312.

ShahA.Z. (2012) Morphology, ultrastructure, and probable functions of the sense organs on the ovipositor stylets of the hymenoptran parasitoid, Venturia canescens (Gravenhorst). Micros. Res. Tech.75876-883.

ShahA.Z.BlackwellA.HubbardS.F. (2012) Ultramorphology of the ovipositor of Venturia canescens (Gravenhorst) and possible mechanisms for oviposition. Int. J. Agric. Biol.14908-914.

Silva-TorresC.S.A.BarrosR.TorresJ.B. (2009) Efeito da Idade, Fotoperíodo e Disponibilidade de Hospedeiro no Comportamento de Parasitismo de Oomyzus sokolowskii Kurdjumov (Hymenoptera: Eulophidae). Neotrop. Entomol.38512-519.

TormosJ.PedroL.BeitiaF.SabaterB.AsísJ.D.PolidoroC. (2013) Development, preimaginal phases and adult sensillar equipament in Aganaspis parasitoids (Hymenoptera: Figitidae) of fruit flies. Microsc. Microanal.191475-1489.

ToscanoL.C.CarvalhoS.L. (2000a) Parasitismo em Pectinophora gossypiella Saunders (Lepidoptera: Gelechiidae) e Anagasta Kuhniella Zeller (Lepidoptera: Pyralidae) por Bracon vulgaris Ashmead (Hymenoptera: Braconidae). Braz. J. Ecol.1223-28.

ToscanoL.C.CarvalhoS.L. (2000b) Parasitismo em Anthonomus grandis Boheman, 1843 por Bracon vulgaris, Ashmead em cultura de algodão sem medidas de controle na região de Ilha Solteira – SP. Braz. J. Ecol.12123-127.

VilhelmsenL. (2003) Flexible ovipositor sheaths in parasitoid Hymenoptera (Insecta). Arth. Struct. & Dev.32277-287.

VilhelmsenL.TurrisiG.F. (2011) Per arborem ad astra: morphological adaptations exploiting the woody habitat in the early evolution of Hymenoptera. Arth. Struct. & Dev.402-20.

WangX.YangZ.GouldJ.R. (2010a) Sensilla on the antennae, legs and ovipositor of Spathius agrili Yang (Hymenoptera: Braconidae), a parasitoid of the emerald ash borer Agrilus planipennis Fairmaire (Coleoptera: Buprestidae). Micros. Res. Tech.73560-571.

WangX.YangZ.GouldJ.R.WuH.MaJ. (2010b) Host-seeking behavior and parasitism by Spathius agrili Yang (Hymenoptera: Braconidae), a parasitoid of the emerald ash borer. Biolog. Control5224-29.

XiaoyiW.ZhongqiY. (2008) Behavioral mechanisms of parasitic wasps for searching concealed insect hosts. Acta Ecol. Sin.281257-1269.

YamamotoM.E.VolpatoG.L. (2007) Comportamento Animal. Primeira edição. Editora UFRNNatal.

ZhouH.WuW.J.NiuL.M.FuY.G. (2013a) Antennal sensilla of female Encarsia guadeloupae Viggiani (Hymenoptera: Aphelinidae), a nymphal parasitoid of the spiraling whitefly Aleurodicus disperses (Hemiptera: Aleyrodidae). Micron44365-372.

ZhouH.WuW.J.ZhangF.P.FuY.G. (2013b) Scanning electron microscopy studies of the antennal sensilla of Metaphycus parasaissetiae Zhang & Huang (Hymenoptera: Encyrtidae). Neotrop. Entomol.42278-287.


  • View in gallery

    Sequence of events related to parasitism behavior of Bracon vulgaris upon Anthonomus grandis: (A) After release, the female wasp remains still (static/stop); (B) The wasp moves towards the vegetal structure, searching for the host (host searching); (C) After contacting the cotton square, the wasp starts grooming; (D) The wasp evaluates the physiological condition (suitability) of the host and its precise location within the cotton square (probing), and (E) The wasp begins oviposition (host acceptance). (F) After parasitism, the female wasp remains inactive on the cotton square (resting).

  • View in gallery

    Scanning electron micrographs of an antenna from a B. vulgaris female. (A) General appearance. Scale bar: 1 mm. (B) Antennal segment detail: scape, pedicel, and flageromeres. Scale bar: 200 μm. (C) Note predominance of trichoid sensilla and layout of basiconical sensilla distally distributed in flageromeres. Scale bar: 200 μm. (D) Third flageromere highlighting the presence of coeloconical sensilla and its lateral location. Scale bar: 30 μm. (E) Trichoid and placode sensilla. Observe the morphology and extension of the placode sensilla, the groove that encircles them, and the cuticular crest around them. Scale bar: 30 μm. (F) Terminal region of the last flageromere; observe the diversity and arrangement of sensilla on the structure. Scale bar: 30 μm. Abbreviations and symbols: E, scape, F, flagelomere; P, pedicel; Sb, basiconical sensilla; St, trichoid sensilla; asterisk, placoid sensilla; arrow, coeloconical sensilla; arrowhead, basal insertion in the trichoid sensilla; dashed arrow, detail of the longitudinal grooves in the trichoid sensilla.

  • View in gallery

    Details of the antennal sensilla of B. vulgaris. (A) Coeloconical sensilla. Scale bar: 2 μm. (B) Placode sensilla. Scale bar: 5 μm. (C) Basiconical sensilla. Scale bar: 10 μm. (D) Insertion of the basiconical sensilla in flagellomeres. Scale bar: 2 μm. (E) Trichoid sensilla. Scale bar: 5 μm. (F) Morphology and thickness of terminations in basiconical and trichoid sensilla. Scale bar: 5 μm. Abbreviations and symbols: ISb, inserting the basiconical sensilla; Sb, basiconical sensilla; St, trichoid sensilla; asterisk, placode sensilla, arrow, coeloconica sensilla, arrowhead, basal insertion of trichoid sensilla with flexible projection.

  • View in gallery

    Electron micrographs of the B. vulgaris ovipositor. (A) General appearance of ovipositor, third valve (V3) or sheath in detail. Scale bar: 1 mm. (B) First and second valves (V1 and V2). Scale bar: 300 μm. (C) Terminal region of valves 1 and 2 in detail, note the juxtaposition of these structures and their morphological divergence and size. Scale bar: 100 μm. (D) V3 dorsal region, observe the unequal subdivisions that add flexibility to the structure. Scale bar: 50 μm. (E) Trichoid sensilla present in the V3 terminal region. Scale bar: 30 μm. (F) Sheath ventral region, observe numerous microtrichia at the apex of the structure. Scale bar: 100 μm. Abbreviations and symbols: S, serrations; Stc, short trichoid sensilla; Stl, long trichoid sensilla; star, microtrichia.


Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 49 49 17
Full Text Views 65 65 40
PDF Downloads 8 8 4
EPUB Downloads 6 6 0