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Citation: Bonifazi, A.; Pacini, M.;
Mancini, E. 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.
Diversity 2022,14, 743. https://
doi.org/10.3390/d14090743
Academic Editor: Luc Legal
Received: 12 August 2022
Accepted: 8 September 2022
Published: 9 September 2022
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diversity
Interesting Images
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
Andrea Bonifazi 1, * , Marta Pacini 1and Emanuele Mancini 2
1ARPA Lazio, Agenzia Regionale per la Protezione Ambientale del Lazio, Dipartimento Stato dell’Ambiente,
00173 Rome, Italy
2Italian Fishery Research and Studies Center, 00184 Rome, Italy
*Correspondence: andrea.bonifazi@arpalazio.it
Abstract:
Oenothera speciosa Nutt. is a non-indigenous plant that is widespread in Europe, South Amer-
ica, 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.
Keywords:
introduced plant; alien species; non-indigenous species; Oenothera speciosa; stuck
proboscis
;
Macroglossum stellatarum; trapped hawkmoths
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
Diversity 2022,14, 743. https://doi.org/10.3390/d14090743 https://www.mdpi.com/journal/diversity
Diversity 2022,14, 743 2 of 7
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).
Diversity 2022, 14, 743 2 of 7
“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 w ere 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).
Figure 1. Two specimens of the hummingbird hawkmoth Macroglossum stellatarum stuck with their
proboscides in the flowers of Oenothera speciosa. In the first picture (a), the flower is newly bloomed,
while in the second picture (b), the flower is wilted, so it can be hypothesized that the moth was
stuck for several hours. Photo credit: Andrea Bonifazi.
Figure 1.
Two specimens of the hummingbird hawkmoth Macroglossum stellatarum stuck with their
proboscides in the flowers of Oenothera speciosa. In the first picture (
a
), the flower is newly bloomed,
while in the second picture (
b
), the flower is wilted, so it can be hypothesized that the moth was stuck
for several hours. Photo credit: Andrea Bonifazi.
Diversity 2022,14, 743 3 of 7
Diversity 2022, 14, 743 3 of 7
Figure 2. Macroglossum stellatarum stuck in the flower of Oenothera speciosa (a) attempting
unsuccessfully to free herself by flapping its wings (b). However, the attempt made the situation
worse, trapping the proboscis even more (c). The last picture (d) shows the proboscis deeply inserted
into the hypanthium of the flower. Photo credit: Andrea Bonifazi.
Figure 3. Two specimens of Macroglossum stellatarum stuck with their proboscides in the flowers of
Oenothera speciosa; the images show that their wings were very damaged in an effort to escape, and
their thoraxes were widely (a) or partially (b) hairless. Photo credit: Andrea Bonifazi.
Figure 2.
Macroglossum stellatarum stuck in the flower of Oenothera speciosa (
a
) attempting unsuc-
cessfully to free herself by flapping its wings (
b
). However, the attempt made the situation worse,
trapping the proboscis even more (
c
). The last picture (
d
) shows the proboscis deeply inserted into
the hypanthium of the flower. Photo credit: Andrea Bonifazi.
Diversity 2022, 14, 743 3 of 7
Figure 2. Macroglossum stellatarum stuck in the flower of Oenothera speciosa (a) attempting
unsuccessfully to free herself by flapping its wings (b). However, the attempt made the situation
worse, trapping the proboscis even more (c). The last picture (d) shows the proboscis deeply inserted
into the hypanthium of the flower. Photo credit: Andrea Bonifazi.
Figure 3. Two specimens of Macroglossum stellatarum stuck with their proboscides in the flowers of
Oenothera speciosa; the images show that their wings were very damaged in an effort to escape, and
their thoraxes were widely (a) or partially (b) hairless. Photo credit: Andrea Bonifazi.
Figure 3.
Two specimens of Macroglossum stellatarum stuck with their proboscides in the flowers of
Oenothera speciosa; the images show that their wings were very damaged in an effort to escape, and
their thoraxes were widely (a) or partially (b) hairless. Photo credit: Andrea Bonifazi.
Diversity 2022,14, 743 4 of 7
Diversity 2022, 14, 743 4 of 7
Figure 4. An exhausted specimen of Macroglossum stellatarum that was stuck in the flower of
Oenothera speciosa for several hours. The proboscis was unrolled and clearly damaged even though
the moths were set free. Photo credit: Andrea Bonifazi.
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
Figure 4.
An exhausted specimen of Macroglossum stellatarum that was stuck in the flower of
Oenothera speciosa
for several hours. The proboscis was unrolled and clearly damaged even though
the moths were set free. Photo credit: Andrea Bonifazi.
On the flowers of O. speciosa, smaller butterflies belonging to the families Papil-
ionidae 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 Tettigoni-
idae), 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 ob-
served 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 pro-
boscis 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.
Diversity 2022,14, 743 5 of 7
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.
Diversity 2022, 14, 743 5 of 7
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.
Figure 5. Some insect species visiting the flowers Oenothera speciosa without showing any damage:
(a) the honeybee Apis mellifera Linnaeus, 1758 (Apidae); the beetles (b) Oxythyrea funesta Poda, 1761
(Scarabaeidae) and (c) Coccinella septempunctata Linnaeus, 1758; and (d) a young katydid (Orthoptera
Tettigoniidae). Photo credit: Andrea Bonifazi.
Figure 5.
Some insect species visiting the flowers Oenothera speciosa without showing any dam-
age: (
a
) the honeybee Apis mellifera Linnaeus, 1758 (Apidae); the beetles (
b
)Oxythyrea funesta Poda,
1761 (Scarabaeidae) and (
c
)Coccinella septempunctata Linnaeus, 1758; and (
d
) a young katydid (Or-
thoptera Tettigoniidae). Photo credit: Andrea Bonifazi.
Diversity 2022,14, 743 6 of 7
Diversity 2022, 14, 743 6 of 7
Figure 6. Section of the trichomal zone of the style (a,b) and hypanthium (c,d) of a flower of
Oenothera speciosa. It is clear as the internal basal part of the hypanthium and the corresponding part
of the style are densely pubescent, and the trichomes are oriented toward the base, with a thick wall
and slightly sigmoid form. Scale bars: (a,c) 100 μm, (b) 50 μm, (d) 30 μm. Photo credit: Andrea
Bonifazi.
Supplementary Materials: The following supporting information can be downloaded at:
www.mdpi.com/xxx/s1. Macroglossum stellatarum stuck in the flower of Oenothera speciosa
attempting unsuccessfully to free herself by flapping vigorously its wings. However, the attempt
makes the situation worse, trapping the proboscis even more. Video credit: Andrea Bonifazi.
Author Contributions: Conceptualization, A.B., M.P. and E.M.; data curation, A.B. and M.P.;
methodology, A.B., M.P. and E.M.; investigation, A.B. and M.P.; validation, A.B., M.P. and E.M.;
visualization, A.B., M.P. and E.M.; writing—original draft preparation, A.B. writing—review and
editing, A.B.; project administration, A.B. All authors have read and agreed to the published version
of the manuscript.
Figure 6.
Section of the trichomal zone of the style (
a
,
b
) and hypanthium (
c
,
d
) of a flower of
Oenothera speciosa.
It is clear as the internal basal part of the hypanthium and the corresponding
part of the style are densely pubescent, and the trichomes are oriented toward the base, with a
thick wall and slightly sigmoid form. Scale bars: (
a
,
c
) 100
µ
m, (
b
) 50
µ
m, (
d
) 30
µ
m. Photo credit:
Andrea Bonifazi.
Supplementary Materials:
The following supporting information can be downloaded at: https:
//www.mdpi.com/article/10.3390/d14090743/s1.Macroglossum stellatarum stuck in the flower
of Oenothera speciosa attempting unsuccessfully to free herself by flapping vigorously its wings.
However, the attempt makes the situation worse, trapping the proboscis even more. Video credit:
Andrea Bonifazi.
Diversity 2022,14, 743 7 of 7
Author Contributions:
Conceptualization, A.B., M.P. and E.M.; data curation, A.B. and M.P.; method-
ology, A.B., M.P. and E.M.; investigation, A.B. and M.P.; validation, A.B., M.P. and E.M.; visualiza-
tion, A.B., M.P. and E.M.; writing—original draft preparation, A.B. writing—review and editing,
A.B.; project administration, A.B. All authors have read and agreed to the published version of
the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Data Availability Statement: Not applicable.
Acknowledgments:
We would like to thank the anonymous reviewers which spent their time to
review our manuscript and to enrich it with their comments. We also thank Andrea Gaion for
correcting the grammar mistakes and much improving the quality of the text. Finally, we thank
Marco Lezzi and Elisabetta Fanti for showing us these places.
Conflicts of Interest: The authors declare no conflict of interest.
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