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Life history traits and interactions of Stylops advarians (Strepsiptera) with its bee host, Andrena milwaukeensis

Published online by Cambridge University Press:  22 January 2020

Zach S. Balzer
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SaskatchewanS7N 5E2, Canada
Arthur R. Davis*
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SaskatchewanS7N 5E2, Canada
*
Author for correspondence: Arthur R. Davis, E-mail: [email protected]

Abstract

Specimens of Stylops advarians were sampled by collecting foraging bees of Andrena milwaukeensis along the South Saskatchewan River within Saskatoon, Saskatchewan. As the foraging season progressed from early May till late June over three consecutive years (2016–2018), most stylopized bees possessed endoparasitic adult (neotenic) females of S. advarians protruding from the bee gaster's dorsum. In contrast, very few adult bees stylopized by male puparia, and no free-living males, were encountered. Over the sampling period, prevalence remained around 22% each year; mean intensity was 1.2 (range of 1–3 female parasites per bee); and parasite abundance was 0.27. Also newly reported for Stylops is the occurrence of one bee bearing four Stylops (two neotenic females and two males with puparia), plus another bee with a male puparium extruded from its gaster's sternites. Around 2 May each year, a high proportion of the earliest captured female bees were stylopized. However, non-stylopized female bees typically were not encountered until about 10 days later, suggesting the parasites manipulate female bee hosts to emerge earlier, in close synchrony to male bee emergence. First-instar larvae of S. advarians appeared from 22–25 May, indicating that adults of S. advarians matured and mated at similar times each season.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Balzer, ZS (2019) Morphology of Stylops advarians (Strepsiptera) and the Effects of Parasitization on its Host, Andrena milwaukeensis (Hymenoptera) (MSc thesis). University of Saskatchewan, Saskatoon, Canada.Google Scholar
Balzer, ZS and Davis, AR (2019a) Adaptive morphology of the host-seeking first-instar larva of Stylops advarians Pierce (Strepsiptera, Stylopidae), a parasite of Andrena milwaukeensis Graenicher (Hymenoptera, Andrenidae). Arthropod Structure & Development 52, 100881.CrossRefGoogle Scholar
Balzer, ZS and Davis, AR (2019b) Description of the adult male of Stylops advarians Pierce (Strepsiptera: Stylopidae). Zootaxa 4674, 496500.CrossRefGoogle Scholar
Beani, L, Cappa, F, Manfredini, F and Zaccaroni, M (2018) Preference of Polistes dominula wasps for trumpet creepers when infected by Xenos vesparum: A novel example of co-evolved traits between host and parasite. PLoS ONE 13, e0205201.CrossRefGoogle ScholarPubMed
Brandenburg, J (1953) Der Parasitismus der Gattung Stylops an der Sandbiene Andrena vaga PZ. Zeitschrift für Parasitenkunde 15, 457475.CrossRefGoogle Scholar
Daly, HV, Doyen, JT and Purcell, AH III (1998) Introduction to Insect Biology and Diversity, 2nd Edn. Oxford, UK: Oxford University Press.Google Scholar
Hrabar, M, Danci, A, McCann, S, Schaefer, PW and Gries, G (2014) New findings on life history traits of Xenos peckii (Strepsiptera: Xenidae). The Canadian Entomologist 146, 514527.CrossRefGoogle Scholar
Hughes, DP, Kathirithamby, J and Beani, L (2004) Prevalence of the parasite Strepsiptera in adult Polistes wasps: field collections and literature overview. Ethology Ecology & Evolution 16, 363375.CrossRefGoogle Scholar
James, M, Nandamuri, SP, Stahl, A and Buschbeck, EK (2016) The unusual eyes of Xenos peckii (Strepsiptera: Xenidae) have green- and UV-sensitive photoreceptors. Journal of Experimental Biology 219, 38663874.CrossRefGoogle ScholarPubMed
Jones, D and Jones, G (1981) Stylopization of Andrena spp. (Hymenoptera: Andrenidae) by Stylops crawfordi (Strepsiptera: Stylopidae) in Texas. Journal of the Kansas Entomological Society 54, 223227.Google Scholar
Jones, D, Williams, ML and Jones, G (1980) The biology of Stylops spp. in Alabama, with emphasis on S. bipunctatae. Annals of the Entomological Society of America 73, 448451.CrossRefGoogle Scholar
Kathirithamby, J (1989) Review of the order Strepsiptera. Systematic Entomology 14, 4192.CrossRefGoogle Scholar
Kathirithamby, J (2009) Host-parasitoid associations in Strepsiptera. Annual Review of Entomology 54, 227249.CrossRefGoogle ScholarPubMed
Kathirithamby, J (2018) Biodiveristy of Strepsiptera. In Foottit, RG and Adler, PH (eds), Insect Biodiversity: Science and Society, Vol. 2. New York, USA: John Wiley & Sons Ltd, pp. 673703.CrossRefGoogle Scholar
Kifune, T and Maeta, Y (1975) A new subgenus and new species of the genus Xenos (Strepsiptera, Stylopidae) from Japan. Kontyû 43, 446455.Google Scholar
Kinzelbach, R (1971) Morphologische Befunde an Fächerflüglern und ihre phylogenetische Bedeutung (Insecta: Strepsiptera). Zoologica 41, 1256.Google Scholar
Kirkpatrick, TW (1937) Studies on the ecology of coffee plantations in East Africa. II. The autecology of Antestia spp. (Pentatomidae) with a particular account of a strepsipterous parasite. Transactions of the Royal Entomological Society of London 86, 247343.CrossRefGoogle Scholar
LaBerge, WE (1980) A revision of the bees of the genus Andrena of the western hemisphere. Part X. Subgenus Andrena. Transactions of the American Entomological Society 106, 395525.Google Scholar
Linsley, EG and MacSwain, JW (1957) Observations on the habits of Stylops pacifica Bohart. The University of California Publications in Entomology 11, 395430.Google Scholar
Maeta, Y (1963) Some biological notes on Pseudoxenos iwatai Esaki (I) its biology and natural history. Kontyû 31, 115.Google Scholar
Maeta, Y (1971) Some biological notes on Pseudoxenos iwatai Esaki (IV) additional notes on its biology and natural history. Kontyû 39, 105119.Google Scholar
Maeta, Y, Gôukon, K, Kitamura, K and Miyanaga, R (2001) Factors that determine the positions where Pseudoxenos iwatai Esaki (Strepsiptera: Stylopidae) extrudes from the host abdomen. Tijdschrift voor Entomologie 144, 203215.CrossRefGoogle Scholar
Makino, S and Yamashita, Y (1998) Levels of parasitism by Xenos moutoni du Buysson (Strepsiptera, Stylopidae) and their seasonal changes in hornets (Hymenoptera, Vespidae, Vespa) caught with bait traps. Entomological Science 1, 537543.Google Scholar
Melber, A (1989) Die Parasitierung der Heidezikade Ulopa reticulata (F.) (Hom., Auchenorrhyncha, Cicadellidae) durch Halictophagus silwoodensis Waloff (Strepsiptera, Halictophagidae) in nordwestdeutschen Calluna-Heiden. Braunschweiger naturkundliche Schriften 3, 419428.Google Scholar
Melber, A and Pohl, H (1997) Erster Nachweis einer Strepsipterenparasitierung bei Wanzen in Mitteleuropa (Insecta, Strepsiptera et Heteroptera). Bonner Zoologische Beiträge 47, 6976.Google Scholar
Peck, SB (1991) Order Strepsiptera, twisted-winged parasites. In Bousquet, Y (ed.), Checklist of Beetles of Canada and Alaska. Ottawa, Canada: Research Branch, Agriculture Canada, pp. 366367.Google Scholar
Pérez, J (1886) Des effets du parasitisme des Stylops sur les apiaries du genre Andrena. Actes de la Société linnéenne de Bordeaux 40, 2163.Google Scholar
Pierce, WD (1909) A monographic revision of the twisted winged insects comprising the order Strepsiptera Kirby. Bulletin of the United States National Museum 66, 1232.Google Scholar
Rivero, A, Giron, D and Casas, J (2001) Lifetime allocation of juvenile and adult nutritional resources to egg production in a holometabolous insect. Proceedings of the Royal Society B – Biological Sciences 268, 12311237.CrossRefGoogle Scholar
Robertson, FW (1957) Studies in quantitative inheritance XI. Genetic and environmental correlation between body size and egg production in Drosophila melanogaster. Journal of Genetics 55, 428443.CrossRefGoogle Scholar
Roy, S and Hazra, N (2016) 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, 8285.Google Scholar
Schenk, M, Mitesser, O, Hovestadt, T and Holzschuh, A (2018) Overwintering temperature and body condition shift emergence dates of spring-emerging solitary bees. PeerJ 6, e4721.CrossRefGoogle ScholarPubMed
Schwartz, MD and Karl, TR (1990) Spring phenology: nature's experiment to detect the effect of ‘green-up’ on surface maximum temperatures. Monthly Weather Review 118, 883890.2.0.CO;2>CrossRefGoogle Scholar
Smith, GW and Hamm, AH (1914) Studies on the experimental analysis of sex – part 11. Quarterly Journal of Microscopial Science 60, 435461.Google Scholar
Straka, J (2019) Strepsiptera of Canada. Zookeys 819, 377382.CrossRefGoogle Scholar
Straka, J, Rezkova, K, Batelka, J and Kratochvíl, L (2011) Early nest emergence of females parasitized by Strepsiptera in protandrous bees (Hymenoptera Andrenidae). Ethology Ecology & Evolution 23, 97109.CrossRefGoogle Scholar
Straka, J, Juzova, K and Nakase, Y (2015) Nomenclature and taxonomy of the genus Stylops (Strepsiptera): an annotated preliminary world checklist. Acta Entomologica Musei Nationalis Pragae 55, 305332.Google Scholar
Ulrich, W (1933) Fang und Züchtung von Strepsipteren. Abderhalden, Handbuch der biologischen Arbeitsmethoden, Abt. 9, 7, 259–237.Google Scholar
Ulrich, W (1956) Unsere Strepsipteren-Arbeiten. Zoologische Beitrage 2, 177255.Google Scholar
Waloff, N (1981) The life history and descriptions of Halictophagus silwoodensis sp.n. (Strepsiptera) and its host Ulopa reticulata (Cicadellidae) in Britain. Systematic Entomology 6, 103113.CrossRefGoogle Scholar
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