The Banyan Leaf Skeletonizer moth, Choreutis sexfasciella (Sauber, 1902) (Lepidoptera: Choreutidae), is reported from Cyprus for the first time from Ficus microcarpa L.fil. and F. benjamina L. trees in urban areas of Larnaca, Limassol, and Paphos. C. sexfasciella was originally described from the Philippines and has rapidly extended its range in the last five years into several Mediterranean countries as well as into North America. DNA barcode sequencing of several specimens from Cyprus has demonstrated that they are closely related to North American specimens. The parasitoid wasp Elasmus cf. cyprianus Ferrière, 1947 (Hymenoptera: Eulophidae) has been reared from leaves infested with larvae of C. sexfasciella. The observed socioeconomic impacts of the non-native moth and the potential use of its parasitoid as a biological control agent are discussed.

Ficus microcarpa L.fil., F. benjamina L. and other Indo-Australian representatives of the genus Ficus L. (Moraceae) have been introduced across the globe as ornamental plants in urban and semi-urban areas and have been followed by a large number of non-native insect species (Barbagallo et al. 2005; Wang et al. 2015a; Laudani et al. 2020; Laarif and Bouslama 2022; van Noort and Rasplus 2023). In Cyprus, these introduced tree species have been extensively planted in urban habitats such as parks, gardens, and roadsides, leading to the accidental introduction and establishment of numerous non-native insects. To date, more than thirty non-native species have been found to be associated with non-native Ficus spp. on the island, including a wide range of phytophagous species (e.g., Hemiptera and Thysanoptera) as well as chalcid wasps forming a paraphyletic group exclusively reproducing within figs, appropriately termed “fig wasps” (EPPO 2014a, b; Collins and Philippou 2016; Compton et al. 2020; Demetriou et al. 2023a; Japoshvili et al. 2023; Koutsoukos et al. 2024).

Species of the genus Choreutis Hübner, 1825 (Lepidoptera: Choreutidae), such as C. aegyptiaca (Zeller, 1867), C. japonica (Zeller, 1877), and C. sexfasciella (Sauber, 1902), are known to be associated with ornamental Ficus spp. (Savela 2019; Abu Ghonem et al. 2020). Choreutis sexfasciella, also known as the Banyan Leaf Skeletonizer (Figure 1), was first described from the Philippines (Semper 1902) and is considered native to parts of the Eastern Palaearctic and Indomalayan biogeographic realms (Rittner 2019; Savela 2019). Nevertheless, the species has managed to escape its native range, even reaching California and Florida in North America (Beucke 2021; Hodel et al. 2021; Hayden et al. 2023; Heppner 2023). In the Mediterranean basin, it has been reported from Israel (Rittner 2019), Egypt (Abu Ghonem et al. 2020), and most recently Türkiye (Can and Koçak 2024), and it is also known from Réunion (Bippus 2020). To date, the only species of the genus known to inhabit Cyprus is C. nemorana (Hübner, 1799), feeding on the native Ficus carica L. (Karsholt and van Nieukerken 2013).

Fig. 1. 

Observed signs of infestation by Choreutis sexfasciella (Sauber, 1902) on Ficus microcarpa L. (A); imago collected from Paphos, Chloraka, Melanos (B); pinned imago (♀) deposited at Lund University, MZLU-00208361 (C).

The non-native species of Choreutis that first appeared in California in 2021 was originally recorded under the name Choreutis emplecta (Turner, 1942) (Beucke 2021; Hodel et al. 2021) as its DNA barcode sequence matched the specimens of this Australian species. In the meantime, the matter was further complicated by Bippus (2020), who transferred C. emplecta into Anthophila Haworth [1811], without providing an explanation for this taxonomic act. This led to some confusion about the correct generic placement for this invasive species. In 2023, Heppner synonymized C. emplecta with C. sexfasciella. As part of our project, we tested both the synonymy hypothesis as well as the generic placement of this species with molecular data.

Parasitoid wasps of the genus Elasmus Westwood, 1833 (Hymenoptera: Eulophidae) are known to parasitize various Diptera, Hymenoptera, and Lepidoptera, although their hosts are largely unknown (Graham 1995; Verma et al. 2002; Yefremova and Strakhova 2012). Known cases of chalcid wasps parasitizing Choreutidae are quite rare, limited only to E. nudus (Nees, 1834), which has been catalogued as a larval and pupal parasitoid of Tebenna bjerkandrella (Thunberg, 1784), and Conura side Walker, 1843, a parasitoid of T. silphiella (Grote, 1881) (Labeyrie 1962; Noyes 2019). In Cyprus, five species of Elasmus have been identified, namely: E. bicolor (Fonscolombe, 1840), E. platyedrae Ferrière, 1935, E. cyprianus Ferrière, 1947, E. phthorimaeae Ferrière, 1947, and E. steffani Viggiani, 1967 (Ferrière 1947; Graham 1995). These species are known parasitoids of moths belonging to numerous lepidopteran families, such as Elachistidae Bruand, 1851, Gelechiidae Stainton, 1854, Erebidae: Lymantriinae Hampson, 1893, Plutellidae Guenée, 1845, Psychidae Boisduval, 1828, Tortricidae Latreille, 1803, and Yponomeutidae Stephens, 1829, which include notorious pests of agricultural plants e.g. Pectinophora gossypiella (Saunders, 1844), Phthorimaea operculella (Zeller, 1873) (Graham 1995), and Prays oleae Bernard, 1788, affecting cotton, potato, and olive production, respectively.

In this study, C. sexfasciella is recorded for the first time in Cyprus, where it is damaging ornamental F. microcarpa foliage in urban habitats of Larnaca, Limassol, and Paphos districts. A parasitoid, Elasmus cf. cyprianus (Fig. 2), was reared from C. sexfasciella larvae, constituting the first known parasitoid for the species. We sequenced one mitochondrial (COI-5P – the DNA barcode) and one nuclear gene from several specimens and combined our sequences with the publicly available data for a phylogenetic analysis. We briefly discuss the relationship of the Cyprus population of C. sexfasciella to the other sequenced populations of this species, test the validity of its synonymy with C. emplecta, and elucidate the taxonomic placement of C. sexfasciella. The impacts of this non-native moth on Ficus spp. in Cyprus, as well as its biological control are also discussed.

Fig. 2. 

Elasmus cf. cyprianus Ferrière, 1947, adult female reared in Limassol, Kato Polemidia from pupae of Choreutis sexfasciella (Sauber, 1902).

During sampling for material in urban areas of Larnaca, Limassol, and Paphos districts in July and August 2021, damaged and withered leaves of F. microcarpa and F. benjamina were observed being covered in small, dark-coloured excrement and silk-web (Fig. 1A). Choreutis sexfasciella larvae were observed resting under silk-webs on the adaxial leaf lamina. Withered leaves with excrement and web evidenced the presence of the larvae, while thick silken cocoons located on the midrib indicated the presence of developing pupae (Abu Ghonem et al. 2020). Adult individuals were sparsely observed on the foliage during the evening hours before nightfall. Infested and healthy fresh leaves were collected and stored in plastic containers until the emergence of imagines (Fig. 1B, C). Imagines were preliminarily identified based on photographic material and species diagnoses in Rittner (2019) and Abu Ghonem et al. (2020), with their identity being molecularly confirmed. Two specimens of Elasmus sp. were also reared from pupae in Limassol district and identified as E. cf. cyprianus (Graham 1995) (Fig. 2).

We sequenced the mitochondrial COI and the wingless gene from all 11 specimens. Based on the analysis of the DNA barcode sequences from these 11 specimens and the additional 13 specimens from BOLD, the specimens of C. sexfasciella from Cyprus are closely related to the specimens from the USA (Fig. 4). All of the haplotypes from Cyprus are grouped together, suggesting that there was likely a single introduction event, and they are not showing any population structure with respect to the different regions of Cyprus. The specimens from Australia, which were previously considered as C. emplecta, show less than 2% divergence from the rest of the specimens from different parts of the world. In the analysis of the Choreutinae dataset, C. sexfasciella is deeply nested within Choreutis, with full branch support from both SH and UFB (Fig. 5).

Fig. 4. 

Maximum likelihood tree from the Choreutis sexfasciella (Sauber, 1902) dataset based on the COI sequences. The numbers next to the branches represent branch support as SH-like approximate likelihood ratio test / ultrafast bootstrap. When branch support by both measures is below the level of statistical significance, it is not shown.

Fig. 5. 

Maximum likelihood tree from the Choreutinae dataset based on DNA sequences from COI and seven nuclear genes (Suppl. material 1). The numbers next to the branches represent branch support as SH-like approximate likelihood ratio test / ultrafast bootstrap. When branch support by both measures is below the level of statistical significance, it is not shown. Type species for genera Anthophila and Choreutis are marked with TS.

Choreutis sexfasciella is reported for the first time from Cyprus, supplementing monitoring efforts on the non-native insects associated with ornamental Ficus spp. on the island, as well as adding a second representative of the family Choreutidae to the entomofauna of Cyprus. By the end of 2024, a total of 30 non-native species of Lepidoptera had been reported from Cyprus [excluding Dichelia cedricola (Diakonoff, 1974), a species of questionable status] (Demetriou et al. 2023b). Since then, two more species have been added to this list, including the presented record of C. sexfasciella as well as the fall armyworm, Spodoptera frugiperda (Smith, 1797), a species included in the EPPO A2 list (EPPO 2023a, b). Rittner (2019) hypothesised that C. sexfasciella may have been introduced to Israel through the import of Asian Ficus spp. The species has probably been introduced to Cyprus as a contaminant of nursery material and/or as contaminant on infested alien fig trees (Ficus spp.) [see introduction pathways of alien species UNEP/CBD/SBSTTA/18/9/Add.1, 26 June 2014, as modified according to Pergl et al. (2020)], from neighbouring Egypt, Israel or straight from the species native range.

A molecular analysis of the Cyprus populations of C. sexfasciella, together with the American, Australian, and Papua New Guinean populations, has shed some light on the invasion history of the species, demonstrating that populations in Europe and North America are closely related. However, questions remain. For example, was the introduction of C. sexfasciella into the Mediterranean a single event that has led to a rapid spread of this species since its hosts are widely grown in the region as ornamentals, or were there a number of separate introductions into different areas through trade in ornamental plants? A far greater sequencing effort, covering the full range, is needed to try to answer these questions. Also, so far, no specimens of C. sexfasciella have been sequenced from the Philippines – the species’ type locality.

Our results support Heppner’s (2023) decision to synonymize C. emplecta with C. sexfasciella. The divergence in the COI sequences is below 2% and there is no clear separation between the Australian specimens and those from the other regions. Likewise, C. sexfasciella is firmly placed within the genus Choreutis based on the mitochondrial and nuclear genes, as its morphology clearly suggests.

Larval stages of C. sexfasciella were responsible for damaging stands of ornamental plants (Fig. 1A) undermining the aesthetics of nature (Kueffer and Kull 2017) and thus indicating some potential socioeconomic impacts of the species. Nevertheless, the extent of the observed damage to the host-plant did not seem to significantly affect the survival of the plants. Despite being commonly used as an ornamental plant, F. microcarpa has escaped urban areas, reaching natural habitats in the Mediterranean basin (Wang et al. 2015b). In invaded habitats, it has also been associated with the destruction of infrastructure and replacement of native flora (Ramírez and Montero 1988; Starr et al. 2003; Wang et al. 2015a), although such outcomes have not been reported from Mediterranean countries. Tsintides et al. (2002) and Demetriou et al. (2023a), document socioeconomic and human-health risks linked to F. microcarpa in Cyprus, including slippery sidewalks and road crossings due to fallen figs as well as damage to cars and pavements.

Elasmus cyprianus was first described from the island by Ferrière (1947), “breeding in young green carob pods” (Graham 1995). Its host species are unknown and presumably belong to some lepidopteran developing in pods of Ceratonia siliqua L. (Graham 1995). Additionally, male individuals of the species have not been described (Ferrière 1947; Graham 1995). The identification of reared samples was performed using the identification key of Graham (1995) and compared with the re-description of morphologically similar species E. phthorimaeae (Strakhova and Yefremova 2010). The reared specimens resemble those of E. cyprianus, although comparison with type material is required (R.R. Askew, pers. comm.). Additional examination of the material using keys for Asian Elasmus provided no results (R.R. Askew, pers. comm.). As such, our samples are identified as E. cf. cyprianus (pedicel longer than F1; F3 approx. 1.3 times as long as broad) unveiling a new, non-native host for the European Elasmus species.

Future research on C. sexfasciella in Cyprus should be carried out in order to map the extent of its distribution, determine other possible host-plants and identify any further adverse impacts. The potential use of E. cf. cyprianus for the biological control of C. sexfasciella could also be assessed by measuring its parasitism rate and seasonal dynamics. Rearing of specimens may provide us with male samples, which are currently undescribed, while the comparison of reared specimens with type material will be conducted once additional individuals are collected.

We are grateful to Dr Richard Robinson Askew and Dr Mark Shaw for their comments and advice regarding the identification of Elasmus and the manuscript. We thank Kristián Grell (Biology Centre of the Czech Academy of Sciences, České Budějovice) for his help with laboratory work during his internship in the Systematic Biology Group at Lund University as well as Milla Ahola (University of Turku, Turku, Finland). We also thank Bjarne Skule (Denmark) for kindly assisting our investigations. We are grateful for being able to access two sequences from the BOLD project LOQT. Some of the sequence data originated from a large rearing project in Papua New Guinea (PNG project) by the Binatang Research Centre, organized by Vojtech Novotny, George Weiblen, Yves Basset, and Scott Miller and funded by the US National Science Foundation and Czech Science Foundation, with sequencing provided by the Biodiversity Institute of Ontario through the International Barcode of Life program funded by Genome Canada. We greatly appreciate the comments and suggestions made by our reviewer Dr Erik van Nieukerken (Naturalis Biodiversity Center, Leiden, Netherlands), subject editor Dr Carlos Lopez Vaamonde (French National Institute for Agriculture, Food, and Environment, Paris, France), as well as Dr David Lees for improving the overall quality of the manuscript. Finally, we are thankful to the UK Government through Darwin Plus (DPLUS124 and DPLUS202), for funding this project.