The Spreading in Europe of the Non-Indigenous Species Oenothera speciosa Nutt. Might Be a Threat to the Autochthonous Moth Macroglossum stellatarum (Linnaeus, 1758)? A New Case Study from Italy

Abstract

Oenothera speciosa Nutt. is a non-indigenous plant that is widespread in Europe, South America, Asia, and Oceania. Although in its native range it is rarely pollinated by sphingid moths, in Europe and Asia, it was found to be associated with the hummingbird hawkmoth Macroglossum stellatarum (Linnaeus, 1758). However, the plant–insect interaction was negative, and the moths were found with proboscides stuck to the flowers of this plant. This interaction is a relevant conservation issue that requires further studies to assess its ecological impact. This work represents the first record of the negative interaction between O. speciosa and M. stellatarum in Italy.

The genus Oenothera (L., 1753), belonging to the family Onagraceae, currently consists of 145 species of flowering plants [1]. These species mainly occur in temperate America as well as in the tropics but also comprise plants native to Europe and established aliens, mostly represented by species escaping from cultivation [2].

Within this genus, Oenothera speciosa Nutt. is an herbaceous perennial species native to prairies in the United States of America and northern Mexico [2,3] and is currently a worldwide-distributed species that is widespread in Europe, South America, Asia, and Oceania [4]. This species is one of the most frequently cultivated Oenothera species and is listed as escaped from cultivation in many areas of the world, where it is reported as a perennial alien introduced as an ornamental plant [5]. In fact, in the past several years, O. speciosa has been expanding its range, and it has recently been reported in many European countries, such as some areas of Spain [6,7], Greece [8], Sweden, Finland [9], Bulgaria [10], and Albania [11], as well as countries in Asia, such as Iraq [12] and China [13].

In Italy, O. speciosa has been reported as a casual alien species in Lombardy, Veneto, Tuscany, and Sicily and as a naturalized alien in Marche and Emilia Romagna, and it often grows in abandoned urban gardens, probably introduced a few years ago for ornamental purposes in small flowerbeds, then expanding to the surrounding areas [14,15]. The flowers of this species bloom between May and July and stay open throughout most of the daytime and at night, except for the hottest hours [16].

Many Oenothera species are usually pollinated by large nocturnal moths, especially those belonging to the family Sphingidae, and have typical sphingophilous adaptations: a deep hypanthium, pale corolla color, spreading four-lobed stigmas elevated above the anthers, fragrance, and nectar [10]. For this reason, these species are considered “hawkmoth flowers”. In fact, sphingid moths have a long proboscis adapted for feeding from specific flowering plants. Although O. speciosa shows these features, in its native countries, it is not usually pollinated by sphingid species but mainly by diurnal insects, such as honeybees, some species of butterflies (e.g., the families Hesperiidae, Papilionidae, and Pieridae), and chrysomelid beetles [16,17]. On the other hand, in countries where O. species is listed as an allochthonous species, some sphingid moths were observed feeding on its flowers. In particular, the Eurasian hummingbird hawkmoth Macroglossum stellatarum (Linnaeus, 1758), a species native to Europe but also distributed in Asia and northern Africa, is a typical diurnal visitor of O. speciosa [10,12].

An interesting negative plant–insect interaction has been documented in France [18,19], Bulgaria [10], and Iraq [12]: some authors have observed that when M. stellatarum inserts its proboscis into the hypanthium of the flowers of O. speciosa, its tubular mouthpart can become physically stuck in the flower, and the moth remains trapped; the trapped insects generally die after a short period, becoming prey for other faunal organisms.

This work represents the first record of the negative interaction between O. speciosa and M. stellatarum in Italy (See Supplementary).

The observations were performed in the late spring, from 9 to 11 June 2022, on private land in Brisighella, Ravenna (44.21124 N, 11.78201 E), a small town located in central northern Italy. In this geographic area, O. speciosa is considered a naturalized allochthonous species and is sometimes spread aggressively by rhizomes and self-seeding colonies [20]. In the investigated area, several bushes of O. speciosa were found near a vineyard, and a total of about 30 flowers were observed. In these few days, a total of nine specimens of M. stellatarum were found stuck in the flowers of O. speciosa, with the proboscides trapped between the tapered hairs of both the hypanthium and the style (Figure 1). All the specimens were found hovering, exhausted or about to die (Figure 2); many specimens showed damaged wings in an effort to escape, and some of them showed a hairless thorax instead of a scale-covered one (Figure 3). Only two moths self-released in a few minutes when picked up with the flowers. The other specimens were not able to free themselves because their proboscides were too stuck and coiled in the hypanthium. Specimens that were probably trapped for several hours, even though they were helped to break free, showed damaged and unrolled proboscides (Figure 4).

On the flowers of O. speciosa, smaller butterflies belonging to the families Papilionidae and Pieridae were also found, along with diurnal bees, such as Apis mellifera Linnaeus, 1758 (Apidae); beetles, such as Oxythyrea funesta Poda, 1761 (Scarabaeidae), Lachnaia italica Weise, 1881 (Chrysomelidae), Coccinella septempunctata Linnaeus, 1758, and Harmonia axyridis (Pallas, 1773) (Coccinellidae); and young katydids (Orthoptera Tettigoniidae), but their visits to the flowers appeared to be trouble-free (Figure 5).

As noted by Alkhesraji et al. (2016) in Iraq and Zlatkov et al. (2018) in Bulgaria, other moth species (e.g., Agrius convolvuli (Linnaeus, 1758), Hyles livornica (Esper, 1780), Sphinx pinastri (Linnaeus, 1758), and Autographa californica (Speyer, 1875)) were also observed stuck to flowers, but they always escaped without external assistance. It should be noted that some of these moth species are considerably larger than M. stellatarum and have longer proboscides. The negative interaction between O. speciosa and M. stellatarum could be attributed to both the inner morphology of the flower and the structure of the proboscis of this moth: in fact, the style and hypanthium are densely covered with trichomes (Figure 6). The trichomes are non-glandular, unicellular, and oriented toward the base, and they have a thick wall and slightly sigmoid form. As highlighted by Zlatkov et al. (2018), the proboscides of M. stellatarum have numerous transverse grooves separating the cuticular annulations, which fit well into the trichome tips; when a moth inserts its proboscis into the flower of O. speciosa, the tips of the trichomes enter the grooves, and the reflex movement of the proboscis is hindered by the orientation of the trichomes.

Although in its native range, O. speciosa is rarely visited by sphingid moths [16,17], and no cases of dead moths with trapped proboscides have been reported in the literature, in 2017, the species M. stellatarum was firstly recorded in California, USA [21]. It might be interesting to know if this negative interaction also occurs in the areas where the plant is indigenous.

To date, we have no data on the impact of O. speciosa on M. stellatarum, but the killing of an autochthonous insect species by causal or naturalized alien plants requires further studies to assess its ecological impact.