Terminal-instar larval morphology and systematics of Eulophidae and Eupelmidae species (Hymenoptera, Chalcidoidea) parasitoids of gall wasps (Hymenoptera, Cynipidae) communities from Europe

in Insect Systematics & Evolution
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.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

As part of a wider study on the morphology and systematics of the terminal-instar larvae of Chalcidoidea parasitoids of gall wasps (Hym., Cynipidae) in Europe, a comparative study of the larval morphology of three species of Eulophidae, Aprostocetus eurytomae (Nees), Aulogymnus skianeuros (Ratzeburg) and Dichatomus acerinus Förster; and three species of Eupelmidae, Eupelmus aseculatus (Kalina), E. cerris Förster and E. microzonus Förster is presented. The studied taxa are key components of the communities associated with different galls on herbs, shrubs and oaks in different ecosystems of Mediterranean area. Main characters of interest found on the studied species were larval body shape, head capsule structure, mouthparts, mandibles and chaetotaxy pattern of body and head. Diagnostic characters of the families and species are described and illustrated for the first time with scanning electron microscopy (SEM). Information on the biology of each species is discussed and illustrated with photographs, including new rearing records.

Terminal-instar larval morphology and systematics of Eulophidae and Eupelmidae species (Hymenoptera, Chalcidoidea) parasitoids of gall wasps (Hymenoptera, Cynipidae) communities from Europe

in Insect Systematics & Evolution

Sections

References

Aguiar A. Deans A.R. Engel M.L. Forshage M. Huber J.T. Jennings J.T. Johnson N.F. Lelej A.S. Longino J.T. Lohrmann V. Mikó I. Ohl M. Rasmussen C. Taeger A. & Yu D.S.K. (2013) Order Hymenoptera. Zootaxa 3703: 5162.

Al khatib F. Fusu L. Cruaud A. Gibson G. Borowiec N. Rasplus J.-Y. Ris N. & Delvare G.  (2014) An integrative approach to species discrimination in the Eupelmus urozonus complex (Hymenoptera, Eupelmidae), with the description of 11 new species from the Western Palaearctic. Systematic Entomology 39: 806862.

Al khatib F. Fusu L. Cruaud A. Gibson G. Borowiec N. Rasplus J.-Y. Ris N. & Delvare G . (2015) Availability of eleven species names of Eupelmus (Hymenoptera, Eupelmidae) proposed in Al khatib et al. (2014) . ZooKeys 505: 137145.

Askew R.R. (1959) Revision of the British species of the genus Olynx Förster (Hym., Eulophidae). Entomologist’s Monthly Magazine 95 (1958): 4957.

Askew R.R. (1961a) Eupelmus urozonus Dalman (Hym. Chalcidoidea) as a parasite in cynipid oak galls. Entomologist 94: 196201.

Askew R.R. (1961b) The biology of the British species of the genus Olynx Förster (Hymenoptera: Eulophidae), with a note on seasonal colour forms in the Chalcidoidea. Proceedings of the Entomological Society of London (Serie A) 36: 103112.

Askew R.R. (1962) The species of Pediobius Walker (Hymenoptera, Eulophidae) inhabiting cynipid oak galls. Entomophaga 7: 337342.

Askew R.R. (1963) Some Chalcidoidea (Hymenoptera) reared from galls of Pediaspis aceris (Förster) (Hym., Cynipidae). Entomologist 96: 273276.

Askew R.R. (1968) Hymenoptera, Chalcidoidea: Elasmidae and Eulophidae (Elachertinae, Eulophinae, Euderinae). Handbooks for the Identification of British Insects. Royal Entomological Society of London 8 (2b). Royal Entomological Society of LondonLondon.

Askew R.R. & Nieves-Aldrey J.L. (2000) The genus Eupelmus Dalman, 1820 (Hymenoptera, Chalcidoidea, Eupelmidae) in peninsular Spain and the Canary Islands, with taxonomic notes and descriptions of new species. Graellsia 56: 4961.

Askew R.R. & Nieves-Aldrey J.L. (2004) Further observations on Eupelminae (Hymenoptera, Chalcidoidea, Eupelmidae) in the Iberian Peninsula and Canary Islands, including descriptions of new species. Graellsia 60: 2739.

Askew R.R. & Nieves-Aldrey J.L. (2006) Calosotinae and Neanastatinae in the Iberian Peninsula and Canary Islands, with descriptions of new species and a supplementary note on Brasema Cameron, 1884 (Hymenoptera, Chalcidoidea, Eupelmidae). Graellsia 62: 87100.

Askew R.R. Plantard O. Gómez J.F. Hernández Nieves M. & Nieves-Aldrey J.L. (2006) Catalogue of parasitoids and inquilines in galls of Aylacini, Diplolepidini and Pediaspidini (Hym., Cynipidae) in West Palaearctic. Zootaxa 1301: 160.

Askew R.R. Melika G. Pujade-Villar J. Schonrogge K. Stone G.N. & Nieves-Aldrey J.L. (2013) Catalogue of parasitoids and inquilines in cynipid oak galls in the West Palaearctic. Zootaxa 3643: 1133.

Baselga A. Lobo J.M. Hortal J. Jiménez-Valverde A. & Gómez J.F. (2010) Assessing alpha and beta taxonomy in Eupelmid wasps: determinants of the probability of describing good species and synonyms. Journal of Zoological Systematics and Evolutionary Research 48: 4049.

Bouček Z. (1965) Studies of European Eulophidae, IV: Pediobius Walk and two allied genera (Hymenoptera). Acta Entomologica Musei Nationalis Pragae 36: 590.

Bouček Z. & Askew R.R. (1968) Palaearctic Eulophidae sine Tetrastichinae . Index of Entomophagous Insects 3 ( Delucchi V. & Remaudière G. Eds). Le François, Paris.

Fagundes Pereira F. Oliveira Kassab S. Rodrigues Ferreira Calado V. Leite Vargas E. Nonato de Oliveira H. & Cola Zanuncio J. (2015) Parasitism and emergence of Tetrastichus howardi (Hymenoptera: Eulophidae) on Diatraea saccharalis (Lepidoptera: Crambidae) larvae, pupae and adults. Florida Entomologist 98: 377380.

Gibson G.A.P. (1995) Parasitic wasps of the subfamily Eupelminae: classification and revision of world genera (Hymenoptera: Chalcidoidea: Eupelmidae). Memoirs on Entomology International. Associated PublishersGainsville, FL.

Gibson G.A.P. Heraty J.M. & Woolley J.B. (1999) Phylogenetics and classification of Chalcidoidea and Mymarommatoidea – a review of current concepts (Hymenoptera, Apocrita). Zoologica Scripta 28: 87124.

Gibson G.A.P. & Fusu L. (2016) Revision of the Palaearctic species of Eupelmus (Eupelmus) Dalman (Hymenoptera: Chalcidoidea: Eupelmidae). Zootaxa 4081: 1331.

Gómez J. F. & Nieves-Aldrey J.L. (2012) Notes on the larval morphology of Pteromalidae (Hymenoptera: Chalcidoidea) species parasitoids of gall wasps (Hymenoptera: Cynipidae) in Europe. Zootaxa 3189: 3955.

Gómez J.F. Hernández Nieves M. Garrido Torres A.M. Askew R.R. & Nieves-Aldrey J.L. (2006) Los Chalcidoidea (Hymenoptera) asociados con agallas de cinípidos (Hymenoptera, Cynipidae) en la Comunidad de Madrid. Graellsia 62: 293331.

Gómez J.F. Hernández Nieves M. & Nieves-Aldrey J.L. (2008) Comparative morphology, biology and phylogeny of terminal-instar larvae of the European species of Toryminae (Hym., Chalcidoidea, Torymidae) parasitoids of gall wasps (Hym. Cynipidae). Zoological journal of the Linnean Society 154: 676721.

Gómez J.F. Nieves-Aldrey J.L. Hernández Nieves M. & Stone G.N. (2011) Comparative morphology and biology of terminal-instar larvae of some Eurytoma (Hym. Eurytomidae) species parasitoids of gall wasps (Hym. Cynipidae) in Western-Europe. Zoosystema 33: 287323.

Gómez J.F. Nieves-Aldrey J.L. & Stone G.N. (2013) On the morphology of the terminal-instar larvae of some European species of Sycophila (Hymenoptera: Eurytomidae) parasitoids of gall wasps (Hymenoptera: Cynipidae). Journal of Natural History 47: 29372960.

Graham M.W.R. de V . (1959) Keys to the British genera and species of Elachertinae, Eulophinae, Entedontinae and Euderinae (Hym., Chalcidoidea). Transactions of the Society for British Entomology 13: 169204.

Graham M.W.R. de V . (1963) Additions and corrections to the British list of Eulophidae (Hym., Chalcidoidea). Transactions of the Society for British Entomology 15: 167275.

Graham M.W.R. de V . (1987) A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain genera. Bulletin of the British Museum (Natural History) (Entomology Series) 55: 1392.

Gumovsky A.V. (2007) A taxonomic revision, biology and morphology of immature stages of the Entedon sparetus species group (Hymenoptera: Eulophidae), egg-larval endoparasitoids of weevils (Coleoptera: Curculionidae). Bulletin of Entomological Research 97: 139166.

Gumovsky A.V. de Little D. Rothmann S. Jaques L. & Ide Mayorga S.E. (2015) Re-description and first host and biology records of Entedon magnificus (Girault & Dodd) (Hymenoptera, Eulophidae), a natural enemy of Gonipterus weevils (Coleoptera, Curculionidae), a pest of Eucalyptus trees. Zootaxa 3957: 577584.

Henneicke K. Dawah H.A. & Jervis M.A. (1992) Taxonomy and biology of the final-instar larvae of some Eurytomidae (Hymenoptera: Chalcidoidea) associated with grasses in the UK. Journal of Natural History 26: 10471087.

LaSalle J. (2005) Biology of Gall Inducers and Evolution of Gall Induction in Chalcidoidea (Hymenoptera: Eulophidae, Eurytomidae, Pteromalidae, Tanaostigmatidae, Torymidae). In: Anantanarayanan R. Schaefer C.W. Withers T.M. (Eds) Biology Ecology and Evolution of Gall-inducing Arthropods. Science PublishersEnfield, NH pp. 507537.

Llácer E. Urbaneja A. Garrrido A. & Jacas J.-A. (2005) Morphology and development of immature stages of Galeopsomyia fausta (Hymenoptera: Eulophidae: Tetrastichinae). Annals of the Entomological Society of America 98: 747753.

MacDonald K.E. & Caveney S. (2004) External morphology and development of immature stages of Elachertus scutellatus (Hymenoptera: Eulophidae) in Florida: the first North American record. Florida Entomologist 87: 559565.

Morris H.M. (1938) Annual report of the entomologist for 1937. In: Annual Report of the Department of Agriculture Cyprus 1937 pp. 4247. Department of AgricultureNicosia.

Muesebeck C.F.W. & Dohanian S.M. (1927) A study in hyperparasitism with particular reference to the parasites of Apanteles melanoscelus (Ratzeburg). Bulletin of U.S. Department of Agriculture 1487. U.S. Department of AgricultureWashington, DC.

Munro J.B. Heraty J.M. Burks R.A. Hawks D. Mottern J. Cruaud A. Rasplus J.-Y. & Jansta P. (2011) A molecular phylogeny of the Chalcidoidea (Hymenoptera). PLoS ONE 6: e27023.

Ndoutoume A. Kalmès R. & Rojas-Rousse D. (2000) Reproductive potential of Eupelmus orientalis (Crawford) and Eupelmus vuilleti (Crawford) (Hymenoptera: Eupelmidae), two parasitoids of Bruchidae (Coleoptera) during the harvest and storage of cowpea pods (Vigna unguiculata (L.) Walp.). African Entomology 8: 201209.

Nieves-Aldrey J.L. (2001) Hymenoptera, Cynipidae. In: Ramos M.A. Alba Tercedor J. Bellés i Ros X. Gosálbez i Noguera J. Guerra Sierra A. Macpherson Mayol E. Martín Piera F. Serrano Marino J. & Templado González J . (Eds) Fauna Ibérica . Vol. 16. Museo Nacional de Ciencias Naturales (CSIC)Madrid.

Nieves-Aldrey J.L. & Askew R.R. (2011) Two new species of Tetrastichinae (Hymenoptera: Eulophidae) from Spain, the first native European gall inducing tetrastichine and its parasitoid. Annales de la Société Entomologique de France 47: 154161.

Nieves-Aldrey J.L. Hernández Nieves M. & Gómez J.F. (2008) Larval morphology and biology of European species of Megastigmus (Hymenoptera, Torymidae, Megastigminae) parasitoids of gall wasps, including a comparison with the larvae of two seed-infesting species. Zootaxa 1746: 4660.

Noyes J.S. (2015) Universal Chalcidoidea Database available online at http://www.nhm.ac.uk/chalcidoids/index.html (accessed 15 March 2015).

Parker H.L. (1924) Recherches sur les formes post-embryonnaires des chalcidiens. Annales de la Société Entomologique de France 93: 262379.

Parker H.L. & Thompson W.R. (1925) Notes on the larvae of the Chalcidoidea. Annals of the Entomological Society of America 18: 384395.

Pujade-Villar J. (1994) Sobre el complejo parasitario (Hym.: Eurytomidae, Pteromalidae, Eulophidae y Eupelmidae) de Pediaspis aceris (Gmelin) (Hym.: Cynipidae) en la Península Ibérica. Boletín de la Asociación española de Entomología18: 2130.

Ranjith A.P. Quicke D.L.J. Saleem U.K.A. Butcher B.A. Zaldívar-Riverón A. & Nasser M. (2016) Entomophytophagy (‘Sequential Predatory, then Phytophagous Behaviour’) in an Indian Braconid ‘Parasitoid’ Wasp (Hymenoptera): Specialized Larval Morphology, Biology and Description of a New Species. PLoS ONE 11: e0156997.

Redfern M. & Askew R.R. (1992) Plant galls. Naturalists’ Handbooks No. 17. Richmond PublishingTotnes.

Roskam J.C. (1982) Larval characters of some eurytomid species (Hymenoptera, Chalcidoidea). Proceedings Koninklijke Nederlandse Akademie van Wetenschappen 85: 293305.

Short J.R.T. (1952) The morphology of the head of larval Hymenoptera with special reference to the head of the Ichneumonoidea, including a classification of the final instar larvae of the Braconidae. Transactions of the Royal Entomological Society of London 103: 2784.

Shorthouse J.D. (1972) An emergence technique for small insects. The Canadian Entomologist 104: 13311332.

Tutin T.G. Heywood V.H. Burges N.A. Valentine D.H. & Moore D.M. (Eds) (1980) Flora Europaea . Vol. 5. Cambridge University Press Cambridge.

Vance A.M. & Smith H.D. (1933) The larval head of Parasitic Hymenoptera and nomenclature of its parts. Annals of Entomological Society of America 26: 8694.

van den Berg E. Prinsloo G.L. & Neser S. (1990) An unusual host association: Aprostocetus sp. (Eulophidae), a hymenopterous predator of the nematode Subanguina mobilis (Chit; Fisher, 1975) Brzeski, 1981 (Anguinidae). Phytophylactica 22: 125127.

Vårdal H. Gómez J.F. & Nieves-Aldrey J.L. (2016) Ovarian egg morphology in chalcidoid wasps (Hymenoptera: Chalcidoidea) parasitizing gall wasps (Hymenoptera: Cynipidae). Graellsia 72: e044.

Figures

  • View in gallery

    General morphology of body in ventral view. (A) Aprostocetus eurytomae (Nees) (Eulophidae); (B) Eupelmus aseculatus (Kalina) (Eupelmidae). Letters refer to the terminology used for general description (see text): ABS1-ABS9, abdominal segments; ANS, anal segment; THS1-THS3, thoracic segments; vlr, ventrolateral region; vmr, ventromedial region.

  • View in gallery

    Body in lateral view. (A) Aprostocetus eurytomae (Nees) (Eulophidae); (B) Eupelmus microzonus Förster (Eupelmidae). Letters refer to the terminology used for general description (see text): ABS1-ABS9, abdominal segments; ANS, anal segment; D, dorsal area of body; epc, spiracles; P, pleural area of body; THS1-THS3, thoracic segments; V, ventral area of body.

  • View in gallery

    Dichatomus acerinus Förster (Eulophidae). (A) Anterior view of head illustrating terminology used for general description (see text). Abbreviations: af, antennal foramina; am, antero-medial setae of antennal area; amf, antero-medial setae on frontal area; an, antenna; anr, antennal area; cl, clypeus; cs, clypeal seate; fr, frons; gn, genal setae; gr, genal region; hr, hypostomal region; hs, hypostomal setae; lb, labrum; vr, vertex region. (B) Anterior view of mouthparts. Abbreviations: cl, clypeus; cs, clypeal setae; lb, labrum; dls, dorso-labral setae; hs, hypostomal setae; lbs, labral setae. The under-lip complex (Mpu) is formed by labium (lbi) and maxillae (mx); Mpu setae: maxillary setae (ms) and antero-medial labial setae (ul).

  • View in gallery

    (A) Anterior view of head of Eupelmus cerris Förster (Eupelmidae) illustrating terminology used for general description (see text). Abbreviations: af, antennal foramina; am, antero-medial setae of antennal region; an, antenna; anr, antennal area; cl, clypeus; cls, clypeal setae; fr, frons; gns, genal setae; gr, genal region; hr, hypostomal region; hs, hypostomal setae; lb, labrum; vam, antero-medial setae of vertex; vr, vertex region. (B) Anterior view of mouthparts of Eupelmus microzonus Förster. Abbreviations: cl, clypeus; cs, clypeal setae; lb, labrum; lcs, latero-clypeal setae. The under-lip complex (Mpu) is formed by labium (lbi), maxillae (mx) and maxillary palps (mp); Mpu setae: maxillary setae (ms) and antero-medial labial setae (ul).

  • View in gallery

    Ventral views of terminal-instar larvae. Eulophidae: (A) Aprostocetus eurytomae; (B) Aulogymnus skianeuros; (C) Dichatomus acerinus. Eupelmidae: (D) Eupelmus aseculatus; (E) Eupelmus cerris; (F) Eupelmus microzonus.

  • View in gallery

    Lateral views of terminal-instar larvae. Eulophidae: (A) Aprostocetus eurytomae; (B) Aulogymnus skianeuros; (C) Dichatomus acerinus. Eupelmidae: (D) Eupelmus aseculatus; (E) Eupelmus cerris; (F) Eupelmus microzonus.

  • View in gallery

    Anterior view of head of terminal-instar larvae. Eulophidae: (A) Aprostocetus eurytomae; (B) Aulogymnus skianeuros; (C) Dichatomus acerinus. Eupelmidae: (D) Eupelmus aseculatus; (E) Eupelmus cerris; (F) Eupelmus microzonus.

  • View in gallery

    Anterior view of mouthparts of terminal-instar larvae. Eulophidae: (A) Aprostocetus eurytomae; (B) Aulogymnus skianeuros; (C) Dichatomus acerinus. Eupelmidae: (D) Eupelmus aseculatus; (E) Eupelmus cerris; (F) Eupelmus microzonus.

  • View in gallery

    Anterior view of the right mandible of terminal-instar larvae. Eulophidae: (A) Aprostocetus eurytomae; (B) Aulogymnus skianeuros; (C) Dichatomus acerinus. Eupelmidae: (D) Eupelmus aseculatus; (E) Eupelmus cerris; (F) Eupelmus microzonus.

  • View in gallery

    (A) terminal-instar larvae of Aprostocetus eurytomae in cell of Diplolepis spinosissimae gall; (B) larva of Eupelmus cerris in galls of Synophrus politus; (C) larvae of Dichatomus acerinus inside cells of Pediaspis aceris gall, sexual generation; (D) galls of Synophrus politus on Quercus suber; (E) galls of sexual generation of Pediaspis aceris on Acer opalus; (F) galls of Diplolepis spinosissimae on Rosa spinossisimae; (G) female of Aulogymnus skianeuros, lateral habitus; (H) female of Eupelmus aseculatus, dorsal habitus; (I) female of Eupelmus cerris (lateral habitus). This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1876312x.

Information

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 51 51 17
Full Text Views 87 87 55
PDF Downloads 4 4 1
EPUB Downloads 0 0 0