Parasitoids (Hymenoptera, Eulophidae, Braconidae) as a Mortality Factor for the Aspen Leafminer Phyllonorycter apparella (Lepidoptera, Gracillariidae) in Its Outbreak Site in Udmurtia

The assemblage of hymenopteran parasitoids associated with the leafminer Phyllonorycter apparella (Lepidoptera: Gracillariidae) developing on the aspen Populus tremula L. was studied near Izhevsk in Udmurtia in 2014–2016. Eighteen species (Hymenoptera: Eulophidae and Braconidae) were reared from Ph. apparella, four of them (Pnigalio mediterraneus, Sympiesis dolichogaster, Chrysocharis phryne, and Neochrysocharis formosus) representing the first records as parasitoids of this pest. Monitoring a steady outbreak site of Ph. apparella revealed an annual increase in the number of species in the parasitoid complex: 6 species in 2014, 9 in 2015, and 16 in 2016. Accordingly, the rate of infestation of the leafminer larvae and pupae increased from 7.4 ± 1.4% in 2014 to 19.6 ± 1.6% in 2016. The dominant parasitoid species changed annually. In 2014 there was only one dominant species, P. circumscriptus (92.4%); in 2015, two dominants: M. frontalis + C. trifasciatus (65.6%); in 2016, three species: C. trifasciatus + C. pictus + M. frontalis (59.5%). The percentage of each species declined in subsequent years. The ratio of ecto- to endoparasitoid species was similar in the three years of research: 1: 1 in 2014, 1: 1.25 in 2015, and 1.29: 1 in 2016. The shares of endoparasitoids in 2014, 2015, and 2016 were 95.1, 50.3, and 56.9%, respectively. The role of endoparasitoids in controlling the leafminer was slightly greater than that of ectoparasitoids.