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Anatomical impact and notes on viviparous development related to infestation by neotenic females of Stylops advarians (Strepsiptera: Stylopidae) on adult female Andrena milwaukeensis (Hymenoptera: Andrenidae)

Published online by Cambridge University Press:  31 May 2021

Zachary S. Balzer  and
Arthur R. Davis Open the ORCID record for Arthur R. Davis [Opens in a new window]
Zachary S. Balzer
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, Saskatchewan, S7N 5E2, Canada Department of Biology, Western University, London, Ontario, N6A 5B7, Canada
Arthur R. Davis*
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, Saskatchewan, S7N 5E2, Canada
*
*Corresponding author. Email: [email protected]
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Abstract

Stylops advarians Pierce (Strepsiptera: Stylopidae) is a prevalent parasite of adult Andrena milwaukeensis Graenicher (Hymenoptera: Andrenidae) in Saskatoon, Saskatchewan, Canada. By dissecting adult bees and examining histological sections, we sought to determine how neotenic females of S. advarians impact female hosts of A. milwaukeensis anatomically. Adult bees with 1–3 females of S. advarians within their gasters were compared to nonstylopised bees (control). The presence of a single female parasite inhibited development of the host’s ovaries. The bee’s foregut shifted laterally when one parasite occupied the gaster and ventrally when two or three were present, thereby reducing the crop’s expandable capacity and the amount of nectar and pollen that stylopised bees can ingest. The midgut and hindgut were less significantly affected by stylopisation. Female parasites typically occupied the host’s gaster dorsolaterally, where each was supported by one of the host’s air sacs. If a third female parasite was present, she resided dorsally along the midline of the host’s gaster, mostly supported by the two female parasites to either side. Asynchronous development within neotenic female parasites was demonstrated, wherein mature first-instar larvae occupied the cephalothorax and abdomen at the same time that the adult female was still supporting multiple embryos.

Type
Research Papers
Information
The Canadian Entomologist , Volume 153 , Issue 4 , August 2021 , pp. 500 - 510
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Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

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Footnotes

Subject editor: Shelley Hoover

References

Ascher, J.S. and Pickering, J. 2020. Bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila) [online]. Discover Life. Available from http://www.discoverlife.org/mp/20q?guid=Apoidea_species Google Scholar
Balzer, Z.S. 2019. Morphology of Stylops advarians (Strepsiptera) and the effects of parasitization on its host, Andrena milwaukeensis (Hymenoptera) [online]. M.Sc. thesis. University of Saskatchewan, Saskatoon, Canada. Available from https://harvest.usask.ca/bitstream/handle/10388/12351/BALZER-THESIS-2019.pdf?sequence=1 Google Scholar
Balzer, Z.S. and Davis, A.R. 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. https://doi.org/10.1016/j.asd.2019.100881.CrossRefGoogle Scholar
Balzer, Z.S. and Davis, A.R. 2019b. Description of the adult male of Stylops advarians Pierce (Strepsiptera, Stylopidae). Zootaxa, 4674: 496–500. https://doi.org/10.11646/zootaxa.4674.4.9.CrossRefGoogle Scholar
Balzer, Z.S. and Davis, A.R. 2020. Life history traits and interactions of Stylops advarians (Strepsiptera) with its bee host, Andrena milwaukeensis . Parasitology, 147: 410–417. https://doi.org/10.1017/S0031182020000037.CrossRefGoogle ScholarPubMed
Balzer, Z.S., Thoroughgood, J.T., Diyes, C.P., Davis, A.R., and Chilton, N.B. 2020. Molecular identification of Stylops advarians (Strepsiptera: Stylopidae) in western Canada. Parasitology Research, 119: 4255–4258. https://doi.org/10.1007/s00436-020-06946-3.CrossRefGoogle Scholar
Benedeczky, I., Tanács, L., and Móczár, L. 1990. Electron microscopic structure of the cephalic gland of the bee Andrena variabilis Smith (Hymenoptera: Apoidea). Acta Biologica Hungarica, 41: 341–361.Google Scholar
Cappa, F., Manfredini, F., Dallai, R., Gottardo, M., and Beani, L. 2014. Parasitic castration by Xenos vesparum depends on host gender. Parasitology, 141: 1080–1087. https://doi.org/10.1017/S003118201400047X.CrossRefGoogle ScholarPubMed
Ceylan, A., Sevin, S., and Özgenc, Ö. 2019. Histomorphological and histochemical structure of the midgut and hindgut of the Caucasian honey bee (Apis mellifera caucasica). Turkish Journal of Veterinary and Animal Sciences, 43: 747–753. https://doi.org/10.3906/vet-1906-55.CrossRefGoogle Scholar
Chapman, G.B. and Abu-Eid, C. 2001. The proventriculus of the carpenter bee, Xylocopa virginica (L.), with special reference to bacteria-containing luminal tunnels. Invertebrate Biology, 120: 78–87. https://doi.org/10.1111/j.1744-7410.2001.tb00028.x.CrossRefGoogle Scholar
Dubitzky, A., Plant, J., and Schönitzer, K. 2010. Phylogeny of the bee genus Andrena Fabricius based on morphology (Hymenoptera: Andrenidae). Mitteilungen der Münchner Entomologischen Gesellschaft, 100: 137–202. https://doi.org/10.14411/eje.2004.045.Google Scholar
Fontaine, C., Dajoz, I., Meriguet, J., and Loreau, M. 2006. Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLOS Biology, 4: 129–135. https://doi.org/10.1371/journal.pbio.0040001.Google ScholarPubMed
Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., Cunningham, S.A., et al. 2013. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339: 1608–1611. https://doi.org/10.1126/science.1230200.CrossRefGoogle ScholarPubMed
Kathirithamby, J. 1989. Review of the order Strepsiptera. Systematic Entomology, 14: 41–92. https://doi.org/10.1111/j.1365-3113.1989.tb00265.x.CrossRefGoogle Scholar
Kathirithamby, J. 2009. Host–parasitoid associations in Strepsiptera. Annual Review of Entomology, 54: 227–249. https://doi.org/10.1146/annurev.ento.54.110807.090525.CrossRefGoogle ScholarPubMed
Kathirithamby, J. 2018. Biodiversity of Strepsiptera. In Insect biodiversity: science and society. Edited by Footit, R.G. and Adler, P.H.. John Wiley & Sons Ltd., New York, New York, United States of America. Pp. 673–703. https://doi.org/10.1002/9781118945582.ch22.CrossRefGoogle Scholar
Kremen, C., Williams, N.M., and Thorp, R.W. 2002. Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Sciences of the United States of America, 99: 16812–16816. https://doi.org/10.1073/pnas.262413599.CrossRefGoogle ScholarPubMed
LaBerge, W.E. 1973. A revision of the bees of the genus Andrena of the western hemisphere. Part VI. Subgenus Trachandrena . Transactions of the American Entomological Society, 99: 235–371.Google Scholar
LaBerge, W.E. 1977. A revision of the bees of the genus Andrena of the western hemisphere. Part VIII. Subgenera Thysandrena, Dasyandrena, Psammandrena, Rhacandrena, Euandrena, Oxyandrena . Transactions of the American Entomological Society, 103: 1–143.Google Scholar
LaBerge, W.E. 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: 395–525.Google Scholar
LaBerge, W.E. and Ribble, D.W. 1972. A revision of the bees of the genus Andrena of the western hemisphere. Part V. Gonandrena, Geissandrena, Parandrena, Pelicandrena . Transactions of the American Entomological Society, 98: 271–358.Google Scholar
Linsley, E.G. and MacSwain, J.W. 1957. Observations of the habits of Stylops pacifica Bohart. University of California Publications in Entomology, 11: 395–430.Google Scholar
Memmott, J., Waser, N.M., and Price, M.V. 2004. Tolerance of pollination networks to species extinctions. Proceedings of the Royal Society B: Biological Sciences, 271: 2605–2611. https://doi.org/10.1098/rspb.2004.2909.CrossRefGoogle ScholarPubMed
Michener, C.D. 2007. The bees of the world. Johns Hopkins University Press, Baltimore, Maryland, United States of America.Google Scholar
Morandin, L.A. and Winston, M.L. 2005. Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecological Applications, 15: 871–881. https://doi.org/10.1890/03-5271.CrossRefGoogle Scholar
Peinert, M., Wipfler, B., Jetschke, G., Kleinteich, T., Gorb, S.N., Beutel, R.G., and Pohl, H. 2016. Traumatic insemination and female counter-adaptation in Strepsiptera (Insecta). Nature Scientific Reports, 6: 25052. https://doi.org/10.1038/srep25052.CrossRefGoogle Scholar
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.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: 21–63.Google Scholar
Santos, C.G. and Serrão, J.E. 2006. Histology of the ileum in bees (Hymenoptera, Apoidea). Brazilian Journal of Morphological Sciences, 23: 405–413.Google Scholar
Serrão, J.E. 2005. Proventricular structure in solitary bees (Hymenoptera, Apoidea). Organisms, Diversity & Evolution, 5: 125–133. https://doi.org/10.1016/j.ode.2004.10.011.CrossRefGoogle Scholar
Smith, G.W. and Hamm, A.H. 1914. Studies on the experimental analysis of sex. Part 11. Quarterly Journal of Microscopical Science, 60: 435–461.Google Scholar
Snodgrass, R.E. 1910. The anatomy of the honey bee. United States Department of Agriculture, Bureau of Entomology, Washington, DC, United States of America. Technical Series 18. 162 pp.Google 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: 92–109. https://doi.org/10.1080/03949370.2011.554880.CrossRefGoogle Scholar
Ulrich, W. 1956. Unsere Strepsipteren-Arbeiten. Zoologische Beitrage, 2: 177–255.Google Scholar
Winfree, R., Reilly, J.R., Bartomeus, I., Cariveau, D.P., Williams, N.M., and Gibbs, J. 2018. Species turnover promotes the importance of bee diversity for crop pollination at regional scales. Science, 359: 791–793. https://doi.org/10.1126/science.aao2117.CrossRefGoogle ScholarPubMed