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Niche differentiation of two pupal parasitoid wasps of Musca domestica (Diptera: Muscidae): Pachycrepoideus vindemmiae and Spalangia endius (Hymenoptera: Pteromalidae)

Published online by Cambridge University Press:  02 June 2021

Sheng Zhang Open the ORCID record for Sheng Zhang [Opens in a new window] ,
Yumei Tao ,
Yongzhuo Chen ,
Pengcheng Liu ,
Jialu Liu  and
Haoyuan Hu
Sheng Zhang
Affiliation:
Collaborative Innovation Centre of Recovery and Reconstruction of Degraded Ecosystem in Wanjiang Basin, co-founded by Anhui Province and Ministry of Education, School of Ecology and Environment, Anhui Normal University, Wuhu241000, Anhui, People’s Republic of China
Yumei Tao
Affiliation:
Collaborative Innovation Centre of Recovery and Reconstruction of Degraded Ecosystem in Wanjiang Basin, co-founded by Anhui Province and Ministry of Education, School of Ecology and Environment, Anhui Normal University, Wuhu241000, Anhui, People’s Republic of China
Yongzhuo Chen
Affiliation:
Collaborative Innovation Centre of Recovery and Reconstruction of Degraded Ecosystem in Wanjiang Basin, co-founded by Anhui Province and Ministry of Education, School of Ecology and Environment, Anhui Normal University, Wuhu241000, Anhui, People’s Republic of China
Pengcheng Liu
Affiliation:
Collaborative Innovation Centre of Recovery and Reconstruction of Degraded Ecosystem in Wanjiang Basin, co-founded by Anhui Province and Ministry of Education, School of Ecology and Environment, Anhui Normal University, Wuhu241000, Anhui, People’s Republic of China
Jialu Liu
Affiliation:
Collaborative Innovation Centre of Recovery and Reconstruction of Degraded Ecosystem in Wanjiang Basin, co-founded by Anhui Province and Ministry of Education, School of Ecology and Environment, Anhui Normal University, Wuhu241000, Anhui, People’s Republic of China
Haoyuan Hu*
Affiliation:
Collaborative Innovation Centre of Recovery and Reconstruction of Degraded Ecosystem in Wanjiang Basin, co-founded by Anhui Province and Ministry of Education, School of Ecology and Environment, Anhui Normal University, Wuhu241000, Anhui, People’s Republic of China
*
*Corresponding author. Email: [email protected]
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Abstract

In nature, competing species often achieve coexistence through niche differentiation. We examined this phenomenon for Pachycrepoideus vindemmiae and Spalangia endius (Hymenoptera: Pteromalidae), two species of pupal parasitoids that are considered biological control agents of house fly, Musca domestica (Diptera: Muscidae). We examined the ability of each species, alone and in combination, to locate host pupae buried at different depths (0, 1, 2, 4, and 6 cm) in three types of substrate (sand, dry wheat bran, and spent fly diet). We then evaluated the competitiveness of each species by allowing first one species, then the other species, to parasitise host individuals within time periods ranging from less than 2 hours to 96 hours of each other. Spalangia endius exhibited greater ability than did P. vindemmiae to locate host pupae buried at depths below one centimetre. Conversely, P. vindemmiae exhibited a greater competitive ability, being more likely to emerge from pupae co-parasitised by S. endius, regardless of oviposition interval or sequence. Our findings suggest that these two parasitoid species coexist through niche differentiation. Our findings also indicate that to increase the effectiveness of biological control, the environmental conditions and risk of interspecific competition should be considered when selecting parasitoid species for release.

Type
Research Papers
Information
The Canadian Entomologist , Volume 153 , Issue 5 , October 2021 , pp. 511 - 523
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© The Author(s), 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

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Footnotes

Subject editor: Kevin Floate

References

Bai, S.F., Li, X., Chen, X.X., Cheng, J.A., and He, J.H. 2011. Interspecific competition between two endoparasitoids Cotesia vestalis (Hymenoptera: Braconidae) and Oomyzus sokolowskii (Hymenoptera: Eulophidae). Archives of Insect Biochemistry and Physiology, 76: 156–167. https://doi.org/10.1002/arch.20399.CrossRefGoogle Scholar
Briggs, C.J. 1993. Competition among parasitoid species on a stage-structured host and its effect on host suppression. The American Naturalist, 141: 372–397. https://doi.org/10.1086/285479.CrossRefGoogle Scholar
Brown, W.L. and Wilson, E.O. 1956. Character displacement. Systematic Zoology, 5: 49–64. https://doi.org/10.2307/2411924.CrossRefGoogle Scholar
Chen, W., He, Z., Ji, X.L., Tang, S.T., and Hu, H.Y. 2015. Hyperparasitism in a generalist ectoparasitic pupal parasitoid, Pachycrepoideus vindemmiae (Hymenoptera: Pteromalidae), on its own conspecifics: when the lack of resource lead to cannibalism. PLOS One, 10: e0124305.CrossRefGoogle Scholar
Chen, Z., Liu, J., He, Z., Duan, B., and Hu, H.Y. 2011. Strategies of Pachycrepoideus vindemmiae parasitizing pupae of houseflies. Chinese Journal of Applied Entomology, 48: 176–179.Google Scholar
Chiel, E. and Kuslitzky, W. 2016. Diversity and abundance of house fly pupal parasitoids in Israel, with first records of two Spalangia species. Environmental Entomology, 45: 283–291. https://doi.org/10.1093/ee/nvv180.CrossRefGoogle ScholarPubMed
Cranshaw, W. and Broberg, A. 2015. Biological control organisms for insects and mites. [online]. Available from https://extension.umd.edu/sites/default/files/_image291s/programs/hgic/Publications/non_HGIC_FS/BIOLOGICAL20CONTROL%20O292RGANISMS%20FOR.pdf [accessed 5 April 2016].Google Scholar
Crespo, J.E., Martinez, G.A., and Castelo, M.K. 2015. Exposure to competitors influences parasitism decisions in ectoparasitoid fly larvae. Animal Behaviour, 100: 38–43. https://doi.org/10.1016/j.anbehav.2014.11.005.CrossRefGoogle Scholar
Cushing, J.M., Levarge, S., Chitnis, N., and Henson, S.M. 2004. Some discrete competition models and the competitive exclusion principle. Journal of Difference Equations Applications, 10: 1139–1151. https://doi.org/10.1080/10236190410001652739.CrossRefGoogle Scholar
Cusumano, A., Peri, E., Vinson, S.B., and Colazza, S. 2012. Interspecific extrinsic and intrinsic competitive interactions in egg parasitoids. Biocontrol, 57: 719–734. https://doi.org/10.1007/s10526-012-9451-5.CrossRefGoogle Scholar
Dayan, T. and Simberloff, D. 2005. Ecological and community-wide character displacement: the next generation. Ecology Letters, 8: 875–894. https://doi.org/10.1111/j.1461-0248.2005.00791.x.CrossRefGoogle Scholar
De Moraes, C.M. and Mescher, M.C. 2005. Intrinsic competition between larval parasitoids with different degrees of host specificity. Ecological Entomology, 30: 564–570. https://doi.org/10.1111/j.0307-6946.2005.00723.x.CrossRefGoogle Scholar
Denoth, M., Frid, L., and Myers, J.H. 2002. Multiple agents in biological control: improving the odds? Biological Control, 24: 20–30. https://doi.org/10.1016/S1049-9644(02)00002-6.CrossRefGoogle Scholar
Dry, F.E., Steinkraus, D.C., Steelman, C.D., McNew, R.W., and McKay, T. 2007. Survey of parasitoids (Hymenoptera: Pteromalidae) of house fly (Diptera: Muscidae) pupae from broiler-breeder poultry houses in northwest Arkansas. Biocontrol Science and Technology, 17: 757–763. https://doi.org/10.1080/09583150701408980.CrossRefGoogle Scholar
Floate, K. and Spooner, R. 2002. Parasitization by pteromalid wasps (Hymenoptera) of freeze-killed house fly (Diptera: Muscidae) puparia at varying depths in media. Journal of Economic Entomology, 95: 908–911. https://doi.org/10.1093/jee/95.5.908.CrossRefGoogle ScholarPubMed
Geden, C.J. 2002. Effect of habitat depth on host location by five species of parasitoids (Hymenoptera: Pteromalidae, Chalcididae) of house flies (Diptera: Muscidae) in three types of substrates. Environmental Entomology, 31: 411–417. https://doi.org/10.1603/0046–225X-31.2.411.CrossRefGoogle Scholar
Geden, C.J. and Skovgård, H. 2014. Status of Tachinaephagus zealandicus (Hymenoptera: Encyrtidae), a larval parasitoid of muscoid flies, in the U.S. and Denmark. Journal of Vector Ecology, 39: 453–456. https://doi.org/10.1111/jvec.12123.CrossRefGoogle Scholar
Gibson, G.A.P. and Floate, K.D. 2004. Filth fly parasitoids on dairy farms in Ontario and Quebec, Canada. The Canadian Entomologist, 136: 407–417. https://doi.org/10.4039/n03-006.CrossRefGoogle Scholar
Godfray, H.C.J. and Godfray, H. 1994. Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton, New Jersey, United States of America.CrossRefGoogle Scholar
Goubault, M.E., Fourrier, J., Krespi, L., Poinsot, D., and Cortesero, A.M. 2004. Selection strategies of parasitized hosts in a generalist parasitoid depend on patch quality but also on host size. Journal of Insect Behavior, 17: 99–113. https://doi.org/10.1023/B:JOIR.0000025135.94296.8d.CrossRefGoogle Scholar
Haccou, P., Glaizot, O., and Cannings, C. 2003. Patch leaving strategies and superparasitism: an asymmetric generalized war of attrition. Journal of Theoretical Biology, 225: 77–89. https://doi.org/10.1016/S0022-5193(03)00223-6.CrossRefGoogle ScholarPubMed
Hafez, M. 1953. On the behavior and sensory physiology of the house-fly larva, Musca domestica L. II. Prepupating stage. Journal of Experimental Zoology, 124: 199–225. https://doi.org/10.1002/jez.1401240202.CrossRefGoogle Scholar
Hardin, G. 1960. The competitive exclusion principle. Science, 131: 1292–1297. https://doi.org/10.1126/science.131.3409.1292.CrossRefGoogle ScholarPubMed
Harvey, J.A., Poelman, E.H., and Tanaka, T. 2013. Intrinsic inter- and intraspecific competition in parasitoid wasps. Annual Review of Entomology, 58: 333–351. https://doi.org/10.1146/annurev-ento-120811-153622.CrossRefGoogle ScholarPubMed
Hawkins, B.A. 2005. Pattern and process in host-parasitoid interactions. Cambridge University Press, Cambridge, United Kingdom.Google Scholar
He, Z., Liu, J.B., Chen, Y.L., Chen, Z.Z., Duan, B.S., and Hu, H.Y. 2013. Effects of different treatment methods of housefly pupae for the reproduction of Pachycrepoideus vindemmiae Rondani. Journal of Applied Ecology, 24: 795–800.Google ScholarPubMed
Hu, H.Y., Chen, Z.Z., Duan, B.S., Zheng, J.T., and Zhang, T.X. 2012. Effects of female diet and age on offspring sex ratio of the solitary parasitoid Pachycrepoideus vindemmiae (Rondani) (Hymenoptera, Pteromalidae). Revista Brasileira de Entomologia, 56: 259–262. https://doi.org/10.1590/S0085-56262012005000028.CrossRefGoogle Scholar
Johnson, C.A. and Bronstein, J.L. 2019. Coexistence and competitive exclusion in mutualism. Ecology, 100: e02708. https://doi.org/10.1002/ecy.2708.CrossRefGoogle ScholarPubMed
King, B. 1997. Effects of age and burial of house fly (Diptera: Muscidae) pupae on parasitism by Spalangia cameroni and Muscidifurax raptor (Hymenoptera: Pteromalidae). Environmental Entomology, 26: 410–415. https://doi.org/10.1093/ee/26.2.410.CrossRefGoogle Scholar
Laing, J.E. and Corrigan, J.E. 1987. Intrinsic competition between the gregarious parasite, Cotesia glomeratus, and the solitary parasite, Cotesia rubecula [Hymenoptera: Braconidae], for their host, Artogeia rapae [Lepidoptera: Pieridae]. Biocontrol, 32: 493–501. https://doi.org/10.1007/BF02373518.Google Scholar
Legner, E.F. 1977. Temperature, humidity and depth of habitat influencing host destruction and fecundity of muscoid fly parasites. Entomophaga, 22: 199–206. https://doi.org/10.1007/BF02377844.CrossRefGoogle Scholar
MacArthur, R.H. 1984. Geographical ecology: patterns in the distribution of species. Princeton University Press, Princeton, New Jersey, United States of America.Google Scholar
Machtinger, E.T., Geden, C.J., Kaufman, P.E., and House, A.M. 2015. Use of pupal parasitoids as biological control agents of filth flies on equine facilities. Journal of Integrated Pest Management, 6: 16.CrossRefGoogle Scholar
Mackauer, M., Michaud, J.P., and Volkl, W. 1996. Host choice by aphidiid parasitoids (Hymenoptera: Aphidiidae): host recognition, host quality, and host value. The Canadian Entomologist, 128: 959–980. https://doi.org/10.4039/Ent128959-6.CrossRefGoogle Scholar
Magdaraog, P.M., Harvey, J.A., Tanaka, T., and Gols, R. 2012. Intrinsic competition among solitary and gregarious endoparasitoid wasps and the phenomenon of “resource sharing”. Ecological Entomology, 37: 65–74. https://doi.org/10.1111/j.1365-2311.2011.01338.x.CrossRefGoogle Scholar
Morawo, T. and Fadamiro, H. 2016. Identification of key plant-associated volatiles emitted by Heliothis virescens larvae that attract the parasitoid, Microplitis croceipes: implications for parasitoid perception of odor blends. Journal of Chemical Ecology, 42: 1112–1121. https://doi.org/10.1007/s10886-016-0779-7.CrossRefGoogle ScholarPubMed
Morgan, P.B., Patterson, R.S., Labrecque, G.C., Weidhaas, D.E., Benton, A., and Whitfield, T. 1975. Rearing and release of the house fly pupal parasite Spalangia endius Walker. Environmental Entomology, 4: 609–611. https://doi.org/10.1093/ee/4.4.609.CrossRefGoogle Scholar
Morin, P.J. 2009. Community ecology. First edition. Blackwell Science, Inc., Malden, Massachusetts, United States of America. 424 pp.Google Scholar
Mucheru, O., Jiang, N., Kongoro, J., Bruce, A., and Schulthess, F. 2009. Intrinsic competition between two oligophagous parasitoids, Sturmiopsis parasitica and Cotesia sesamiae, attacking the same life stages of lepidopteran cereal stemborers. Entomologia Experimentalis et Applicata, 130: 10–20. https://doi.org/10.1111/j.1570–7458.2008.00788.x.CrossRefGoogle Scholar
Pawson, B., Petersen, J., and Holtzer, T. 1987. Competitive parasitism of house fly pupae (Diptera: Muscidae) by Muscidifurax zaraptor and Urolepis rufipes (Hymenoptera: Pteromalidae). Journal of Medical Entomology, 24: 66–70.CrossRefGoogle Scholar
Penaflor, M.F.G.V., Erb, M., Miranda, L.A., Werneburg, A.G., and Bento, J.M.S. 2011. Herbivore-induced plant volatiles can serve as host location cues for a generalist and a specialist egg parasitoid. Journal of Chemical Ecology, 37: 1304–1313. https://doi.org/10.1007/s10886-011-0047-9.CrossRefGoogle Scholar
Peters, R.S. 2011. Two ways of finding a host: a specialist and a generalist parasitoid species (Hymenoptera: Chalcidoidea: Pteromalidae). European Journal of Entomology, 108: 565–573. https://doi.org/10.14411/eje.2011.073.CrossRefGoogle Scholar
Poelman, E.H., Gols, R., Gumovsky, A.V., Cortesero, A.M., Dicke, M., and Harvey, J.A. 2014. Food plant and herbivore host species affect the outcome of intrinsic competition among parasitoid larvae. Ecological Entomology, 39: 693–702. https://doi.org/10.1111/een.12150.CrossRefGoogle Scholar
R Core Team. 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.Rproject.org.Google Scholar
Roscoe, L.E., Lyons, D.B., Ryall, K.L., and Smith, S.M. 2016. Courtship sequence and evidence of volatile pheromones in Phasgonophora sulcata (Hymenoptera: Chalcididae), a North American parasitoid of the invasive Agrilus planipennis (Coleoptera: Buprestidae). The Canadian Entomologist, 148: 151–162. https://doi.org/10.4039/tce.2015.52.CrossRefGoogle Scholar
Rueda, L. and Axtell, R. 1985. Effect of depth of house fly pupae in poultry manure on parasitism by six species of Pteromalidae (Hymenoptera). Journal of Entomological Science, 20: 444–449.CrossRefGoogle Scholar
Schoener, T.W. 1974. Resource partitioning in ecological communities. Science, 185: 27–39. https://doi.org/10.1126/science.185.4145.27.CrossRefGoogle ScholarPubMed
Schoener, T.W. 1983. Field experiments on interspecific competition. The American Naturalist, 122: 240–285. https://doi.org/10.1086/284133.CrossRefGoogle Scholar
Skovgård, H. 2006. Search efficiency of Spalangia cameroni and Muscidifurax raptor on Musca domestica pupae in dairy cattle farms in Denmark. Biocontrol, 51: 49–64.CrossRefGoogle Scholar
Stiling, P. and Cornelissen, T. 2005. What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biological Control, 34: 236–246. https://doi.org/10.1016/j.biocontrol.2005.02.017.CrossRefGoogle Scholar
Tormos, J., Beitia, F., Böckmann, E.A., Asís, J.D., and Fernández, S. 2009. The preimaginal phases and development of Pachycrepoideus vindemmiae (Hymenoptera, Pteromalidae) on Mediterranean fruit fly, Ceratitis capitata (Diptera, Tephritidae). Microscopy Microanalysis, 15: 422.CrossRefGoogle Scholar
Valente, C., Afonso, C., Goncalves, C.I., and Branco, M. 2019. Assessing the competitive interactions between two egg parasitoids of the Eucalyptus snout beetle, Gonipterus platensis, and their implications for biological control. Biological Control, 130: 80–87. https://doi.org/10.1016/j.biocontrol.2018.10.002.CrossRefGoogle Scholar
Van Alebeek, F., Rojasrousse, D., and Leveque, L. 1993. Interspecific competition between Eupelmus vuilleti and Dinarmus basalis, two solitary ectoparasitoids of Bruchidae larvae and pupae. Entomologia Experimentalis et Applicata, 69: 21–31. https://doi.org/10.1111/j.1570-7458.1993.tb01724.x.CrossRefGoogle Scholar
Van Alphen, J.J.M. and Visser, M.E. 1990. Superparasitism as an adaptive strategy for insect parasitoids. Annual Review of Entomology, 35: 59–79. https://doi.org/10.1146/annurev.en.35.010190.000423.CrossRefGoogle ScholarPubMed
Van Lenteren, J.C. 2012. The state of commercial augmentative biological control: plenty of natural enemies but a frustrating lack of uptake. Biocontrol, 57: 1–20. https://doi.org/10.1007/s10526-011-9395-1.CrossRefGoogle Scholar
Wang, X.G., Kacar, G., Biondi, A., and Daane, K.M. 2016. Foraging efficiency and outcomes of interactions of two pupal parasitoids attacking the invasive spotted wing drosophila. Biological Control, 96: 64–71. https://doi.org/10.1016/j.biocontrol.2016.02.004.CrossRefGoogle Scholar
Wang, X.G. and Messing, R.H. 2003. Intra- and interspecific competition by Fopius arisanus and Diachasmimorpha tryoni (Hymenoptera: Braconidae), parasitoids of tephritid fruit flies. Biological Control, 27: 251–259. https://doi.org/10.1016/S1049-9644(03)00027-6.CrossRefGoogle Scholar
Wang, X.G. and Messing, R.H. 2004a. Two different life-history strategies determine the competitive outcome between Dirhinus giffardii (Chalcididae) and Pachycrepoideus vindemmiae (Pteromalidae), ectoparasitoids of cyclorrhaphous Diptera. Bulletin of Entomological Research, 94: 473–480. https://doi.org/10.1079/BER2004318.CrossRefGoogle Scholar
Wang, X.G. and Messing, R.H. 2004b. The ectoparasitic pupal parasitoid, Pachycrepoideus vindemmiae (Hymenoptera: Pteromalidae), attacks other primary tephritid fruit fly parasitoids: host expansion and potential non-target impact. Biological Control, 31: 227–236. https://doi.org/10.1016/j.biocontrol.2004.04.019.CrossRefGoogle Scholar
Yamamoto, D., Henderson, R., Corley, L.S., and Iwabuchi, K. 2007. Intrinsic, inter-specific competition between egg, egg–larval, and larval parasitoids of plusiine loopers. Ecological Entomology, 32: 221–228.Google Scholar
Zhan, Y., Zhou, M., He, Z., Chen, Z., Duan, B., Hu, H., and Xiao, H. 2013. Effects of host size and parasitism sequences on the parasitism strategies of Spalangia endius. Acta Ecologica Sinica, 33: 3318–3323. https://doi.org/10.5846/stxb201203260409.CrossRefGoogle Scholar