Parasitoids of Heterogynis Rambur ( Lepidoptera : Zygaenoidea , Heterogynidae )

Nine parasitoids of the moth genus Heterogynis are presented: six species of Hymenoptera from the families Chalcididae, Eulophidae and Ichneumonidae (Agrothereutes hospes (Tschek), Baryscapus endemus (Walker), Brachymeria inermis (Fonscolombe), Diplazon laetatorius (F.), Itoplectis maculator (F.) and Trichomalopsis heterogynidis Graham), and three Diptera, family Tachinidae (Compsilura concinnata (Meigen), Exorista segregata (Rondani) and Phryxe hirta (Bigot)). Two of these species, Trichomalopsis heterogynidis and Phryxe hirta, are oligophagous parasitoids specialized on the genus Heterogynis. We also identified two newly recorded parasitoids of Heterogynis: Brachymeria inermis (Chalcididae) and Diplazon laetatorius (Ichneumonidae).


INTRODUCTION
Heterogynis Rambur is the only genus within the family Heterogynidae Hampson and it comprises about 15 species [1][2][3], distributed in Europe and the Maghreb region of North Africa.The best known and well-investigated species is certainly H. penella (Hubner), which is nowadays considered a species complex with geographically isolated populations in spatially narrowly-defined habitats [4].Data on the parasitoids of Heterogynis have been published in a few papers [5][6][7], while some sporadic information can be found in Herting [8], Ford and Shaw [9], and Ford et al. [10].
Heterogynis species are usually not considered as agricultural or forest pests, apart from the newly described H. zikici de Freina, which was observed to defoliate almost completely Chamaecytisus heuffelii on the Vlasina Plateau, Serbia, in 2016.In a previous work, Žikić et al. [7] cited the Heterogynis species found in Serbia as H. sondereggeri de Freina, but it was subsequently identified as spec.nov.H. zikici [11].
However, most Heterogynis parasitoid communities have not been studied yet in detail.
Herein we present all known parasitoids that have been reared from Heterogynis species, revealing relevant information on their biology, other hosts and distribution.

MATERIALS AND METHODS
Of about 15 Heterogynis species recorded in the Western Palearctic, we observed six of them where parasitoids were registered: H. paradoxa Rambur, (Fig. 1 A), H. canalensis Chapman, (Fig. 1 B, Figs 2 C, D), H. penella (Hubner) (Fig. 1 C), H. chapmani de Freina (Fig. 1 E), H. zikici de Freina (Fig. 1 D, Fig. 2 A) and H. eremita Zilli, Cianchi, Racheli and Bullini (Fig. 1 F).To present the parasitoid community of Heterogynis we combined literature and original data.Parasitoids were reared in laboratory conditions from previously caught Heterogynis larvae.The larvae were put into plastic containers covered with muslin cloth to allow ventilation.Ecloded parasitoids were subsequently collected and conserved in 98% ethanol.The information used from the articles is cited in the Introduction.The compiled results are presented in Table 1.Original data are marked with an asterisk (*).
The trophic associations established between parasitoids and Heterogynis species are given in Table 1.
Distribution: present on all continents except Antarctica [17].
Distribution: Compsilura concinnata is recorded throughout Europe, except for Belarus, Estonia, Fin- land, Iceland, Latvia, Lithuania and Norway.It is also widespread in Russia and Asia: China, Georgia, India, Indonesia, Iran, Israel, Japan, Korea, Lebanon, Pakistan and Turkey.In Africa, it is only recorded from Morocco, in America from Barbados, Canada and USA, and also in Australia [34][35][36][37].

DISCUSSION
This contribution to parasitoids of the largely underinvestigated genus Heterogynis represents the first comprehensive compilation of data and new, original records.Of nine parasitoids listed in Table 1, seven have already been reported in several countries.The two newly recorded parasitoids are Brachymeria inermis and Diplazon laetatorius, both emerging from pupae of H. zikici.The finding of D. laetatorius as a parasitoid of H. zikici could be an erroneous record, because some experts emphasize that this parasitoid is specialized to parasitize only hover flies [30].On the other hand, D. laetatorius has also been sporadically reported from some Coleoptera and Lepidoptera [26][27][28]; see the list of other host families in the results.
According to our results it seems that Phryxe hirta is a generalist with regard to Heterogynis species, since it was found on seven taxa, considering H. penella as a different taxon.
From the nine species we report as parasitoids of Heterogynis species, seven are more or less common parasitoids of many other lepidopteran host.However, two species, Trichomalopsis heterogynidis and Phryxe hirta, specialize in only parasitizing Heterogynis species.Nevertheless, T. heterogynidis can hyperparasitize P. hirta when they find themselves in the same host individual.
We can say with some certainty that the specimen of Diplazon laetatorius emerged from one of the collected pupae of H. zikici since we collected the caterpillars and pupae by hand.However, there exists a small possibility that a syrphid larva came in the rearing box with the branches of the host plant.Considering that the sampling site for this species is accessible to authors of this article, we can investigate if the host range of D. laetatorius also includes other insect groups, except Syrphidae.

Funding:
This research was supported by Grant III43001 of the Ministry of Education, Science and Technological Development of the Republic of Serbia.

Table 1 .
List of parasitoids of Heterogynis species found in Europe.