The Diversity and Biology of the Indian Strepsiptera with a Pictorial Key
DOI:
https://doi.org/10.55446/IJE.2023.1364Keywords:
Strepsiptera diversity, biology, endoparasite, key, hypermetamorphosis, primary larva, stylopization, ecology, distribution, IndiaAbstract
Strepsiptera is a monophyletic group of entomophagous, obligate endoparasites, stylopising a wide range of insect hosts belonging to 34 families of Zygentoma, Polyneoptera, Paraneoptera, and Holometabola. So far 30 species in 14 genera and six families of Strepsiptera are known from India. The zoogeographic distribution of the Indian species of Strepsiptera and their known hosts are presented. The biology of Halictophagus australensis Perkins has been explored in detail. Stylopisation of Cofana spectra Distant (Hemiptera: Cicadellidae) by H. australensis lengthens the life span of C. spectra. A pictorial key to the Indian species of Strepsiptera is presented.
Downloads
Metrics
Downloads
Published
How to Cite
Issue
Section
References
Backus E, Hunter W B, Arne C N. 1988. Technique for staining leafhopper (Homoptera: Cicadellidae) salivary sheaths and eggs within unsectioned plant tissue. Journal of Economic Entomology 81(6): 1819-1823.
Baliga H. 1967. A new species of Corioxenos (Stylopedia) parasitising Antestiopsis cruciata (F.) (Homoptera: Pentatomidae). Bulletin of Entomological Research 57: 387-393.
Barrion A T, Litsinger J A. 1983. Parasites of white rice leafhopper Cofana spectra (Dist.) (Hemiptera: Cicadellidae) in the Philippines. International Rice Research Newsletter 8(6): 20.
Beani L, Dallai R, Mercati D, Cappa F, Giusti F, Manfredini F. 2011. When a parasite breaks all the rules of a colony: morphology and fate of wasps infected by a strepsipteran endoparasite. Animal Behaviour 82(6): 1305-1312.
Beani L, Marchini D, Cappa F, Petrocelli I, Gottardo M, Manfredini F, Giusti F, Dallai R. 2017. Subtle effect of Xenos vesparum (Xenidae, Strepsiptera) on the reproductive apparatus of its male host: Parasite or parasitoid? Journal of Insect Physiology 101: 22-30.
Beani L, Dallai R, Cappa F, Manfredini F, Zaccaroni M, Lorenzi M C, Mercati D. 2021. A Strepsipteran parasite extends the lifespan of workers in a social wasp. Scientific Reports 11: 7235.
Benda D, Pohl H, Nakase Y, Beutel R, Straka J. 2022. A generic classification of Xenidae (Strepsiptera) based on the morphology of the female cephalothorax and male cephalotheca with a preliminary checklist of species. Zookeys 1093: 1-134.
Beutel R G, Friedrich F, Hörnschemeyer T, Pohl H, Hünefeld F, Beckmann F, Meier R, Misof B, Whiting M F, Vilhelmsen L. 2011. Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola. Cladistics 27: 341-355.
Beutel R G, Pohl H, Yan E V, Anton E, Liu S-P, Ślipiński A, McKenna D, Friedrich F. 2019. The phylogeny of Coleopterida (Hexapoda) – morphological characters and molecular phylogenies. Systematic Entomology 44: 75-102.
Beutel R G, Friedrich F, Economo E P. 2022. Patterns of morphological simplification and innovation in the megadiverse Holometabola (Insecta). Cladistics 38: 227-245.
Bohart R M. 1943. New species of Halictophagus with a key to the genus in North America (Strepsiptera, Halictophagidae). Annals of the Entomological Society of America 36(3): 341-359.
Boussau B, Walton Z, Delgado J A, Collantes F, Beani L, Stewart I J, Cameron S A, Whitfield J B, Johnston J S, Holland P W, Bachtrog D, Kathirithamby J, Huelsenbeck J P. 2014. Strepsiptera, phylogenomics and the long branch attraction problem. PLoS One 9(10): e107709.
Chattopadhyay A K, Chaudhuri P K. 1980. Record of genus Caenocholax (Myrmecolacidae, Strepsiptera) from India. Journal of the Bombay Natural History Society 76: 490-492.
Chaudhuri P K, Das Gupta S K, Chatterjee A K. 1978. Description of a new species of Parastylops (Strepsiptera, Stylopidae) from Arunachal Pradesh. Oriental Insects 12: 387-389.
Chaudhuri P K, Das Gupta S K. 1979. New species of Halictophagus and Triozocera [Strepsiptera from West Bengal, India]. Oriental Insects 13(1-2): 133-137.
Chaudhuri P K, Ghosh M, Das Gupta S K. 1983. Notes on Indian Strepsiptera with descriptions of three new species. Deutsche Entomologische Zeitschrift 30: 23-29.
Chaudhuri P K, Mazumdar A. 2000. On the biology of Halictophagus australensis Perkins, 1905 from India (Strepsiptera, Halictophagidae). Mitteilungenausdem Museum für Naturkunde in Berlin Deutsche Entomologische Zeitschrift 47(2): 203-215.
Cook J L. 2019. Annotated catalogue of the order Strepsiptera of the World. Transactions of the American Entomological Society 145 (2): 121-267.
Cvačka J, Jiroš P, Kalinová B, Cerná K, Šebesta P, Tomčala A, Vašíčková S, Jahn U, Šobotník J. 2012. Stylopsal: the first identified female-produced sex pheromone of Strepsiptera. Journal of Chemical Ecology 38: 1483-1491.
Dougherty E R, Carlson C, Bueno V M, Harris N C. 2016. Paradigms for parasite conservation. Conservation Biology 30: 724-733.
Esaki T, Hashimoto S. 1931. Report on the leaf–hoppers injurious to the rice plant and their natural enemies. Publications of the Entomological laboratory of the Kyushu Imperial University 2: 39-52.
Fischer S, Laue M, Müller C H G, Meinertzhagen I A, Pohl H. 2021. Ultrastructural 3D reconstruction of the smallest known insect photoreceptors: The stemmata of a first instar larva of Strepsiptera (Hexapoda). Arthropod Structure and Development 62: 101055.
Gillespie J J, McKenna C H, Yoder M J, Gutell R R, Johnston J S et al. 2005. Assessing the odd secondary structural properties of nuclear small subunit ribosomal RNA sequences (18S) of the twisted–wing parasites (Insecta: Strepsiptera). Insect Molecular Biology 14: 625-643.
Hayward A, McMahon DP, Kathirithamby J. 2011. Cryptic diversity and female host specificity in a parasitoid where the sexes utilize hosts from separate orders. Molecular Ecology 20(7): 1508-1528.
Hrabar M, Danci A, McCann S, Schaefer PW, Gries G. 2014. New findings on life history traits of Xenos peckii (Strepsiptera: Xenidae). The Canadian Entomologist 146(5): 514-527.
Hrabar M, HuiMin Z, Gries R, Schaefer PW, Draper J, Britton R, Gries G 2015. (7E,11E)-3,5,9,11- tetramethyltridecadienal: sex pheromone of the strepsipteran Xenos peckii. Journal of Chemical Ecology 41: 732-739.
Hui P, Mukherjee B, Hazra N. 2023. A new species of the genus Tridactylophagus Subramaniam, 1932 from West Bengal, India with a tentative phylogeny and world key to known males (Strepsiptera: Halictophagidae). Zootaxa 5230(3): 296-304.
Johnston S J, Ross L D, Beani L, Hughes D P, Kathirithamby J. 2004. Tiny genomes and endoreduplication in Strepsiptera. Insect Molecular Biology 13: 581-585.
Jurine M. 1816. Observations sur le Xenos vesparum Rossi. Memorie della Accademia delle Scienze di Torino. Classe di Scienze Fisiche, Matematiche e Naturali 23: 1-14.
Kathirithamby J. 1989. Review of the order Strepsiptera. Systematic Entomology 14: 41-92. Kathirithamby J. 2009. Host–parasitoid associations in Strepsiptera. Annual Review of Entomology 54: 227-249.
Kathirithamby J. 2023. World Strepsiptera Database. Accessed at https://strepsiptera.aphia.org on 2023–02–09. doi:10.14284/484 (accessed on 10.02.2023)
Kathirithamby J, Ponnamma V K. 2000. Halictophagus palmae sp. nov. parasitic in Proutista moesta (Westwood) a vector of phytoplasma of palms in India. Journal of South East Asian Natural History 5: 101-105.
Kathirithamby J, Smith D S, Lomas M, Luke B M. 1984. Apolysis without ecdysis in larval development of a strepsipteran, Elenchus tenuicornis (Kirby). Zoological Journal of the Linnaean Society 82: 335-343.
Kathirithamby J, Simpson S, Solulu T, Caudwell R. 1998. Strepsiptera parasites - novel biocontrol tools for oil palm integrated pest management in Papua New Guinea. International Journal of Pest Management 44: 127-133.
Kathirithamby J, Ross L D, Johnston J S. 2003. Masquerading as self? Endoparasitic Strepsiptera (Insecta) enclose themselves in host-derived epidermal bag. PNAS 100 (13): 7655-7659.
Kathirithamby J, Hrabar M, Delgado J A, Collantes F, Dötterl S, Windsor D, Gries G. 2015. We do not select, nor are we choosy: reproductive biology of Strepsiptera (Insecta). Biology Journal of the Linnean Society 116: 221-238.
Kinzelbach R K. 1971. Morphologische befunde an fächerflüglern und ihre phylogenetische bedeutung (Insecta: Strepsiptera). Zoologica 119: 129-256.
Kinzelbach R K. 1975. Die fächerflägler des Senckenberg–Museums III. Pseudoxenos ropalidiae n. sp. Senckenbergiana Biologica 56: 69-73.
Kinzelbach R K. 1978. Strepsiptera. Veb Gustav Fisher Verlag Jena 1: 166 pp. Kirby W. 1802. Monographia apum Angliae, Volume 2. Printed for the author by J Raw, London, U K. 388 pp.
Kogan M. 2012. Two new species of Halictophagidae (Insecta: Strepsiptera) from the Brazilian Amazon Basin. Zootaxa 3517: 79-87.
Kogan M, Poinar G O. 2019. Fossil Strepsiptera (Insecta) of the Poinar Amber collection with description of one new genus and 12 new Neotropical species in the families Protelencholacidae, Elenchidae, and Myrmecolacidae. History of Biology 57: 1-62.
Kristensen N P. 1981. Phylogeny of insect orders. Annual Review of Entomology 26: 135-157.
Lefèvre T, Lebarbenchon C, Gauthier-Clerc M, Missé D, Poulin R, Thomas F. 2009a. The ecological significance of manipulative parasites. Trends in Ecology and Evolution 24(1): 41-48.
Lefèvre T, Adamo S A, Biron D G, Missé D, Hughes D, Thomas F. 2009b. Invasion of the body snatchers: the diversity and evolution of manipulative strategies in host-parasite interactions. Advances in Parasitology 68: 45-83.
Lu X, Liu X. 2014. Discovery of the twisted-wing parasite family Myrmecolacidae (Insecta: Strepsiptera) from China, with description of two new species of the genus Myrmecolax Westwood, 1861. Zootaxa 3881(4): 385-395.
Luna de Carvalho E. 1985. Estrepsipteros da Macaronesia (Insecta Strepsiptera). Boletim da Sociedade Portuguesa de Entomologia. Supplement 1: 63-73.
Maxwell-Lefroy H. 1909. Indian insect life. A manual of the insects of the plains (Tropical India). H Maxwell–Lefroy. Entomologist, Imperial Department of Agriculture for India; Agricultural Research Institute, Pusa. Calcutta and Simla, 1909. pp. xii, 786. Pls. lxxxiv. and Figs. 536.
Maxumdar A, Chaudhuri P K. 1999. Strepsiptera insects of the genus Tridactylophagus Subramaniam from India (Strepsiptera: Halictophagidae). Journal of South Asian Natural History 4(1): 13-17.
Mazumdar A, Chaudhuri P K. 1997. Report of three genera of Strepsiptera (Insecta) from India with description of a new species of Halictophagus Curtis. The Entomologist 116: 218-223.
Mazumdar A, Chaudhuri P K. 2004. A catalogue of strepsipteran species (Insecta) of India. Proceedings of the Zoological Society Calcutta, 57(1): 43-46.
McMahon D P, Hayward A, Kathirithamby J. 2011. The first molecular phylogeny of Strepsiptera (Insecta) reveals an early burst of molecular evolution correlated with the transition to endoparasitism. PLoS ONE 6: e21206.
Misof B, Liu S, Meusemann K, Peters R S, et al. 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346: 763-767.
Misra C S. 1917. The Indian sugar cane leaf-hopper, Pyrilla aberrans Kirby. Memoir of Department of Agriculture India (Entomology series) 5: 73-133.
Niehuis O, Hartig G, Grath S, Pohl H, Lehmann J, Tafer H, Donath A, Krauss V, Eisenhardt C, Hertel J, Petersen M, Mayer C, Meusemann K, Peters R S., Stadler P F., Beutel R G., Bauer E B, McKenna D D., Misof B. 2012. Genomic and Morphological Evidence Converge to Resolve the Enigma of Strepsiptera. Current Biology 22(14): 1309-1313.
Perkins R C L. 1905. Leafhoppers and their natural enemies (Pt. III Stylopidae). Report of work of the experimental station, Hawaiian Sugar Planters Association 1: 91-109. Perkins R C L. 1918a. Further notes on Stylops and stylopized bees. Entomologist’s Monthly Magazine 54: 67-76.
Perkins R C L. 1918b. The assembling and pairing of Stylops. Entomologist’s Monthly Magazine 54: 129-31.
Peters R S, Meusemann K, Petersen M, et al. 2014. The evolutionary history of holometabolous insects inferred from transcriptome based phylogeny and comprehensive morphological data. BMC Evolutionary Biology 14: 52.
Pierce W D. 1909. A monographic revision of the twisted winged insects comprising the order Strepsiptera Kirby. Bulletin of the United States National Museum 66: 1-232.
Pierce W D. 1911. Notes on insects of the order Strepsiptera with descriptions of new species. Proceedings of the United States National Museum 40: 487-511.
Pierce W D. 1914. Description of two new species of Strepsiptera parasitic on sugar cane insects. Proceedings of the Entomological Society of Washington 16: 126-129.
Pohl H. 2002. Phylogeny of the Strepsiptera based on morphological data of the first instar larvae. Zoologica Scripta 31: 123-134.
Pohl H, Beutel R G. 2004. Fine structure of adhesive devices of Strepsiptera (Insecta). Arthropoda Structure and Development 33: 33-43.
Pohl H, Beutel R G. 2005. The phylogeny of Strepsiptera (Hexapoda). Cladistics 21: 328-374. Pohl H, Beutel R G. 2008. The evolution of Strepsiptera (Hexapoda). Zoology (Jena, Germany) 111: 318-338.
Pohl H, Beutel R G. 2013. The Strepsiptera-Odyssey: the history of the systematic placement of an enigmatic parasitic insect order. Systematics and Phylogeny 1 (e4): 17-26.
Pohl H, Wipfler B, Boudinot B, Beutel R G. 2021. On the value of Burmese amber for understanding insect evolution: Insights from †Heterobathmilla-an exceptional stem group genus of Strepsiptera (Insecta). Cladistics 37: 211-229.
Reissig W H, Heinrichs E A, Litsinger J A, Moody K, Fiedler L, Mew T W, Barrion A T. 1986. Illustrated guide to integrated pest management in rice in Tropical Asia (Los Baños, Philippines: International Rice Research Institute).
Rossi P. 1793. Observations de M. Rossi sur un nouveau genre d’Insecte, voisin des Ichneumons. Bulletin de la Socittt Philomathique de Paris 1: 44.
Roy S. 2018. Systematics and life history strategies of Strepsipteran parasitoids (Insecta: Strepsiptera) with their effects on Hemipteran hosts. Ph D Thesis. The University of Burdwan, India.
Roy S, Hazra N. 2016a. Record of a new species of the genus Viridopromontorius Luna de Carvalho (Strepsiptera: Corioxenidae) from India with a revised key to Corioxenidae. Zootaxa 4154: 567-573.
Roy S, Hazra N. 2016b. Seasonal variation of stylopization on white leafhopper Cofana spectra (Distant) (Homoptera: Cicadellidae) by Halictophagus australensis Perkins (Strepsiptera: Halictophagidae). Journal of Entomology and Zoology Studies 4(2): 82-85.
Roy S, Hazra N. 2016c. Two new species of Halictophagidae (Insecta: Strepsiptera) including the first record of the genus Coriophagus Kinzelbach from India. Zootaxa 4189(1): 581-587.
Roy S, Hazra N. 2017. Two new species of Myrmecolacidae (Strepsiptera) with first record of the genus Stichotrema Hofeneder from India. Annales de la Société Entomologique de France 53: 334-343.
Smith D S, Kathirithamby J. 1984. Atypical ‘fibrilla’ flight muscle in Strepsiptera. Tissue and Cell 16(6): 929-940.
Solulu T M, Simpson S J, Kathirithamby J. 1998. The effect of strepsipteran parasitism on a tettigoniid pest of oil palm in Papua New Guinea. Physiological Entomology 23: 388-398.
Subramanian T V. 1927. A new genus and species of the Strepsiptera from South India, Indoxenos membraciphaga gen. and sp. nov. Transactions of the Royal Entomological Society of London 75: 131-135.
Subramaniam T V. 1932. On a new genus and species of Strepsiptera. Records of the Indian Museum 34: 43-46.
Tolasch T, Kehl S, Dötterl S. 2012. First sex pheromone of the order Strepsiptera: (3R,5R,9R)-3,5,9-trimethyldodecanal in Stylops melittae KIRBY, 1802. Journal of Chemical Ecology 38(12): 1493–1503.
Tröger D, Veit G, Beutel R G, Pohl H. 2020. The endoparasitic larval stages of Eoxenos laboulbenei: an atypical holometabolan development (Strepsiptera, Mengenillidae). Arthropod Structure and Development 56: 100932.
Tröger D, Stark H, Beutel R G. 2023. The morphology of the free-living females of Strepsiptera (Insecta). Journal of Morphology 284(6): e21576.
Ulrich W. 1943. Die Mengeiden (Mengenillini) und die phylogenie der Strepsipteren. Z. Parasitenkde 13: 62-101.
Wiegmann B M, Trautwein M D, Kim J W, Cassel B K, Bertone M A, Winterton S L, Yeates D K. 2009. Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biology 7: 34.
Weingardt M, Beutel R G, Pohl H. 2023. Xenos vesparum (Strepsiptera: Xenidae)-A new insect model and its endoparasitic secondary larva. Insect Systematics and Diversity 7(1): 1-40.
Yang C K. 1955. Descriptions of a new species of Strepsiptera parasitic on the rice leafhoppers. Acta Entomologica Sinica 5: 327-333.
Yang C K. 1964. Notes on the new subfamily Tridactylophaginae (Strepsiptera: Halictophagidae). Acta Entomologica Sinica 13: 607-613.
