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Taxonomic issues related to biological control prospects for the ragweed borer, Epiblema strenuana (Lepidoptera: Tortricidae)

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The ragweed borer, Epiblema strenuana (Walker, 1863), has a long history of use as a biological control agent against important weed pests in the family Asteraceae. Recently, E. strenuana has been reported feeding on the invasive perennials Ambrosia confertiflora and A. tenuifolia in Israel. The geographic location of Israel has raised concern over the possibility that the moth may spread to areas such as Ethiopia where the oil-seed crop Guizotia abyssinica is cultivated, as this is a potential host for E. strenuana. However, the taxonomic status of E. strenuana and a current synonym, E. minutana (Kearfott, 1905) is unclear. These taxa have been treated as separate species in the past, and they potentially have different feeding habits and damage different parts of the plant. We analyzed DNA data and adult morphology and determined that E. minutana, stat. rev., is a valid species which we raise from synonymy with E. strenuana. Wing coloration, the shape of the female sterigma, and COI DNA barcodes are consistently different between the two species. We also determined that the species previously identified as E. strenuana in Israel is actually E. minutana. While detailed host range tests have been conducted on the E. strenuana populations released in Australia and China, the host range of E. minutana remains to be clarified. We discuss the history of biological control using E. strenuana and the implications for finding E. minutana in Israel. We also provide species redescriptions for E. strenuana and E. minutana and illustrate diagnostic characters.
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ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN 1175-5334 (online edition)
Accepted by J.W. Brown: 12 Dec. 2019; published: 30 Jan. 2020 347
Zootaxa 4729 (3): 347–358
https://www.mapress.com/j/zt/
Copyright © 2020 Magnolia Press Article
https://doi.org/10.11646/zootaxa.4729.3.3
http://zoobank.org/urn:lsid:zoobank.org:pub:7153F6DE-1DFE-4F55-B10A-E0D3E5ADE016
Taxonomic issues related to biological control prospects for the ragweed borer,
Epiblema strenuana (Lepidoptera: Tortricidae)
TODD M. GILLIGAN1*, DONALD J. WRIGHT2, RICHARD L. BROWN3, BENNO A. AUGUSTINUS4,5 & URS
SCHAFFNER5
1USDA-APHIS-PPQ-Science & Technology, Identification Technology Program, Fort Collins, CO 80526, USA; *Email: todd.
m.gilligan@usda.gov
23349 Morrison Avenue, Cincinnati, OH 45220, USA
3Mississippi State University, W. L. Giles Distinguished Professor, Director, Mississippi Entomological Museum, Mississippi State, MS
39762, USA
4University of Fribourg, Chemin du Musée 10, CH-1700 Fribourg, Switzerland
5CABI, Rue des Grillons 1, CH-2800 Delémont, Switzerland
Abstract
The ragweed borer, Epiblema strenuana (Walker, 1863), has a long history of use as a biological control agent
against important weed pests in the family Asteraceae. Recently, E. strenuana has been reported feeding on the
invasive perennials Ambrosia confertiflora and A. tenuifolia in Israel. The geographic location of Israel has raised
concern over the possibility that the moth may spread to areas such as Ethiopia where the oil-seed crop Guizotia
abyssinica is cultivated, as this is a potential host for E. strenuana. However, the taxonomic status of E. strenuana
and a current synonym, E. minutana (Kearfott, 1905) is unclear. These taxa have been treated as separate species
in the past, and they potentially have different feeding habits and damage different parts of the plant. We analyzed
DNA data and adult morphology and determined that E. minutana, stat. rev., is a valid species which we raise from
synonymy with E. strenuana. Wing coloration, the shape of the female sterigma, and COI DNA barcodes are consis-
tently different between the two species. We also determined that the species previously identified as E. strenuana in
Israel is actually E. minutana. While detailed host range tests have been conducted on the E. strenuana populations
released in Australia and China, the host range of E. minutana remains to be clarified. We discuss the history of
biological control using E. strenuana and the implications for finding E. minutana in Israel. We also provide species
redescriptions for E. strenuana and E. minutana and illustrate diagnostic characters.
Introduction
The ragweed borer, Epiblema strenuana (Walker, 1863), has a long history of use as a biological control agent
against important weed pests in the family Asteraceae. A native of North America, this species has been introduced
to Australia to control Parthenium hysterophorus L. (McFayden 1985; McClay 1987) where it subsequently also
attacked the invasive weed Ambrosia artemisiifolia L. (Dhileepan and McFayden 2012), and in China to control A.
artemisiifolia (Wan et al. 1995; Zhou et al. 2014). The moth was also considered for field release as a biological
control agent in India and South Africa, but it was rejected due to its ability to complete development on the oil-seed
crop Guizotia abyssinica (L.f.) Cass. under laboratory conditions (Jayanth 1987; McConnachie 2015).
Recently, E. strenuana has been reported from Israel, possibly due to an accidental introduction with grain from
the U.S.A. (Yaacoby and Seplyarsky 2011). In Israel, the moth has been found feeding on the invasive perennials
Ambrosia confertiflora DC and Ambrosia tenuifolia Sprengel. The discovery of the moth in Israel has raised con-
cern over the possibility that it may spread to areas where G. abyssinica is cultivated (e.g., Ethiopia). However, the
taxonomic status of E. strenuana and a current synonym, E. minutana (Kearfott, 1905) is unclear. These taxa have
been treated as separate species in the past (e.g., Brown 1973; Blanchard 1979), and they potentially have different
feeding habits and damage different parts of the plant (Stegmaier 1971). Thus, the effectiveness of using E. strenu-
GILLIGAN ET AL.
348 · Zootaxa 4729 (3) © 2020 Magnolia Press
ana as a biological control agent and reducing the risk of non-host target feeding relies on the correct identification
of this species and the taxonomic status of E. minutana.
Taxonomic history
The taxonomic history of E. strenuana and its synonyms, including E. minutana, is long and confusing. Walk-
er (1863) described Grapholita strenuana and G. exvagana in the same publication from “North America.” Two
years later, Clemens (1865) described Steganoptycha flavocellana from Virginia and probably Pennsylvania and
noted differences in size and coloration between individuals. Zeller (1875) described Grapholita subversana from
specimens collected by Boll in Texas and sent to him for identification from the Museum of Comparative Zoology.
Fernald (1882) synonymized all of the aforementioned names under Paedisca strenuana in his catalogue of North
American tortricids, and later (Fernald 1903) transferred strenuana to Eucosma. Heinrich (1923) was the first North
American researcher to examine genitalia for nearly every tortricid species in his taxonomic revisions. Heinrich
(1923) resurrected many of the genera synonymized by Walsingham (1914) under Eucosma and placed them in the
subfamily Eucosminae. Included in this group of taxa was Epiblema, which Heinrich defined by the clasper on the
valva in the male genitalia (Gilligan et al. 2014). Using this character, Heinrich (1923) assigned approximately 30
species, including strenuana, to Epiblema.
Eucosma minutana was described by Kearfott (1905) from “about forty specimens” from North Carolina, Ohio,
Pennsylvania, Maryland, Illinois, Tennessee, and New Jersey. Kearfott (1905) stated that these specimens were
mixed with E. strenuana, but were smaller and had differences in wing coloration and markings. He also noted that
these species were likely not congeneric with E. circulana, the type species of Eucosma, and would eventually be
placed in a different genus. Heinrich (1923) synonymized E. minutana with E. strenuana, stating that E. strenuana
is one of the most variable species in the genus but that this variability could be found in the same series of reared
specimens. He did note, however, that E. minutana specimens were the most distinct based on color. The two spe-
cies remained synonyms until Blanchard (1979) compared a series of individuals he collected from North Padre
Island, Texas with a series of Kearfott’s E. minutana types. Blanchard (1979) determined that E. minutana could be
separated from E. strenuana by its smaller size and narrower wings, as well as differences in the female genitalia:
shape of the sterigma, size of the signa, and shape of the corpus bursae. Based on this evidence, Blanchard (1979)
elevated E. minutana to species status. He also noted that Brown (1973) had reached the same conclusions in his
unpublished Master’s thesis several years prior. Brown (1973) cited the following differences as reasoning for
separating the two species: the forewing color of E. minutana is lighter gray with brown scales absent, whereas E.
strenuana is darker gray with lines of brown scales extending from the apical costal strigulae; the socii of the male
genitalia are shorter in E. minutana than in E. strenuana; the female sterigma in E. minutana is laterally rounded
with narrow lateral flanges and relatively shorter compared to that of E. strenuana, which has straight lateral mar-
gins, wide flanges that turn inwards, and is relatively longer; and the female corpus bursae of E. strenuana has two
signa that are wide and laterally curved, whereas in E. minutana the signa are narrow and nearly straight. Brown
(1973) also cited evidence from a rearing study conducted by Stegmaier (1971) on Lepidoptera, Diptera, and Hy-
menoptera associated with Ambrosia artemisiifolia in Florida. Stegmaier (1971) reared two tortricids, E. strenuana
and “Epiblema sp. not strenuana,” and described differences in their feeding habits. Epiblema strenuana bored into
the stem terminals, producing a fusiform swelling and infesting nearly every terminal, while the other species bored
into the main stem and sometimes the lateral branches but did not infest the terminals or produce fusiform swell-
ing (Stegmaier 1971). Specimens reared from the main stem were later identified as E. minutana by C. P. Kimball
(Brown 1973).
Miller and Pogue (1984) attempted to resolve the taxonomic status of E. minutana using an allometric analysis.
They conducted measurements of adult characters examined by previous authors (e.g., Blanchard 1979) and plotted
these against insect size for 101 specimens collected from the eastern United States. Characters measured included:
forewing length, forewing width, male valval neck width, male socius length, female signa base diameter, and the
female sterigma length-width ratio (Miller and Pogue 1984). Forewing length was used to represent overall insect
size. They concluded that all of the differences in measurements were effectively continuous and correlated with
forewing length, and thus overall size (Miller and Pogue 1984). In addition, they hypothesized that the differences
in feeding observed by Stegmaier (1971) could be explained by variance in host tissue nutritive value or chemical
characteristics. Their final conclusion was that these findings may warrant returning E. minutana to synonymy with
TAXONOMY OF RAGWEED BORER Zootaxa 4729 (3) © 2020 Magnolia Press · 349
E. strenuana (Miller and Pogue 1984). However, Powell (1983) had already synonymized the two species in the
new North American checklist, although he provided no explanation for this change. The two species were treated
as the E. strenuana “complex” by Miller (1987) and Gilligan et al. (2008), and listed as synonyms in subsequent
catalogues (Brown 2005; Gilligan et al. 2018) and checklists (Pohl et al. 2018).
History of biological control
During field surveys in the native range of Parthenium hysterophorus in the late 1970s, E. strenuana was prioritized
as a biological control candidate for this weed in Australia (McClay 1987). Based on the results of host range tests
conducted in its native range and in Australia, the moth was approved for field release in 1982 and subsequently
released in Queensland (McFadyen 1985; McClay 1987). It became established, spread over Queensland and New
South Wales, and is now considered one of the most prominent biological control agents of P. hysterophorus in
Australia (Dhileepan and McFayden 2012), thereby improving rangeland productivity (Dhileepan 2007). In its
introduced range in Australia, E. strenuana also attacks the invasive weeds A. artemisiifolia L. and Xanthium oc-
cidentale Bertol. Ambrosia artemisiifolia is currently considered to be under good control in Queensland and New
South Wales, with E. strenuana feeding cited as a major factor for this success (Gerber et al. 2011).
The Australian E. strenuana population served as source for introductions to China in 1990–1993 (Wan et al.
1995; Ma et al. 2008). Subsequent host range tests revealed that E. strenuana can complete its life cycle on a local
variety of sunflower in no-choice conditions; however, the risk of economic damage to sunflowers was deemed to
be low (Wan et al. 1995). The moth is now established in South, East, Central, and North China, without reports of
sunflower yield losses due to E. strenuana (Ma et al. 2008). In addition to A. artemisiifolia and P. hysterophorus,
E. strenuana also feeds on Xanthium strumarium L. and Ambrosia trifida L. in China. Efforts to control A. artemi-
siifolia in China by biological means is built on synergistic feeding of the leaf beetle Ophraella communa LeSage
(Coleoptera: Chrysomelidae) and E. strenuana, and mass-rearing programs for both species are now in place to
increase their impact on this noxious weed (Zhou et al. 2014).
While E. strenuana is successfully used as a biological control agent on two different continents against two
different target weeds, its relatively broad host range has led to the rejection of its release in India and South Af-
rica. In both cases, the reason for concern was its capacity to feed on G. abyssinica. This plant, originating from
the Ethiopian highlands, is grown as an oil crop in eastern Africa and India. Laboratory host range tests indicated
that E. strenuana will attack this plant in the field, which led to the rejection of its release in India in 1987 (Jayanth
1987). In South Africa, G. abyssinica is not cultivated on a commercial scale; however, the possibility of the moth
spreading to eastern Africa eventually led to concerns about its host range. This led to no-choice experiments of
E. strenuana on various Ethiopian cultivars of G. abyssinica, and initial larval feeding severely damaged all tested
cultivars. As a matter of responsibility, E. strenuana was deprioritized as a potential biological control agent of P.
hysterophorus in South Africa (McConnachie, 2015).
Summary
Although Miller and Pogue (1984) provided a convincing case for a continuous gradient of morphological charac-
ters between E. strenuana and E. minutana, there do seem to be diagnosable differences (e.g., wing coloration) in
the majority of specimens that may indicate these are different species. Molecular data, including DNA barcoding
(Hebert et al. 2003), has been used successfully to resolve taxonomic issues where morphological characters are
ambiguous and to determine which morphological characters are taxonomically informative (e.g., Brown et al.
2014, Gilligan et al. 2014, Gilligan et al. 2016). Here we use DNA barcoding combined with morphology and host
preference to examine populations of the E. strenuana complex from North America, Australia, China, and Israel.
We revise the taxonomy of this group and provide recommendations regarding the use of E. strenuana as a biologi-
cal control agent.
Materials and Methods
We examined 123 adult specimens together with 43 associated genitalia preparations deposited in the following col-
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350 · Zootaxa 4729 (3) © 2020 Magnolia Press
lections: The Natural History Museum, London, United Kingdom (BMNH); Essig Museum of Entomology, Univer-
sity of California, Berkeley, California, U.S.A. (EME); Florida State Collection of Arthropods, Gainesville, Florida,
U.S.A. (FSCA); Mississippi Entomological Museum, Mississippi State University, Starkville, Mississippi, U.S.A.
(MEM); and National Museum of Natural History, Washington, D.C., U.S.A. (USNM). Specimens from popula-
tions in Australia, China, and Israel were obtained from Dr. Kunjithapatham Dhileepan (Australia), Dr. Zhongshi
Zhou (China), and Nadav Nussbaum (Israel), and sent to US and TMG in ethanol.
Images of adults were taken with Canon 100 mm and MP-E 65 mm macro lenses attached to a Canon 7D digital
SLR. Images of genitalia were taken with a Nikon DS-Fi2 digital microscope camera attached to a Nikon Eclipse 80i
compound microscope. All images were edited using Photoshop CS6 or CC, and some are composite stacks of many
individual images created with Zerene Stacker. Forewing length (FWL) is defined as the distance from the base to
the apex including the fringe, reported to the nearest half millimeter. The forewing aspect ratio (AR) is defined as the
forewing length divided by the medial forewing width. Measurements were made with a stereomicroscope equipped
with an ocular micrometer or a compound microscope using a slide micrometer. The number of observations sup-
porting a particular statistic is indicated by “n =.” Dissection methods follow those presented in Brown and Powell
(1991), and morphological nomenclature follows Horak (2006) and Gilligan et al. (2008, 2014).
Sequences generated for this study were produced using the following methods: DNA was extracted from
crushed legs or abdomens soaked overnight in lysis buffer and proteinase K using a Qiagen DNeasy Blood and
Tissue Kit (Qiagen, Valencia, Calif.) following the manufacturer’s recommended protocol. PCR reactions were
performed with TaKaRa Ex Taq HS polymerase (Takara Bio, Shiga, Japan) in total volumes of 50 µl using the
manufacturer’s recommended volumes of 10X Ex Taq buffer and dNTP mixture. The primers LepF1/LepR1 (Hebert
et al. 2004) were used to amplify a 658bp segment of cytochrome c oxidase I (COI) on a Bio-Rad C1000 Touch
(Bio-Rad Laboratories, Inc., Hercules, Calif.). PCR conditions included an initial denaturation step of 94°C (3min),
39 cycles of 94°C (20 sec)/ 50°C (20 sec)/ 72°C (30 sec), and an extension step of 72°C (5 min). Amplicons were
purified using a Qiaquick PCR Purification Kit and eluted into 35 µl of EB buffer. Sequencing was performed at
the University of Chicago Cancer Research Center DNA Sequencing Facility using an Applied Biosystems 3730XL
DNA sequencer (Applied Biosystems, Foster City, California). Individual forward and reverse contigs were as-
sembled using Geneious Prime 2019 (Biomatters Ltd., Auckland, New Zealand), manually trimmed, and examined
for errors.
An additional 55 publically available sequences for Epiblema that we could confidently assign to the E. strenu-
ana complex were downloaded from the Barcode of Life Data System website (BOLD; Ratnasingham and Hebert
2007). These were combined with 24 newly generated sequences and two sequences of E. foenella from BOLD that
were used to root the tree. All sequences (81 total) were aligned with MAFFT ver. 6 using the G-INS-i algorithm
(Katoh et al. 2002). A maximum likelihood analysis was performed using Garli ver. 2.0 (Zwickl 2006) and the GTR
+ gamma nucleotide substitution model. Optimal likelihood trees were obtained using 1,000 independent searches.
Results and Discussion
The most optimal likelihood tree constructed with the DNA barcoding data is illustrated in Figure 1. Sequences
from the E. strenuana complex fall into two primary clades (Group 1 and Group 2). Group 1 contains sequences
from specimens originating from Australia, Canada (Ontario, Québec), China, Jamaica, Taiwan, and the United
States (Alabama, Connecticut, Illinois, Maryland, Ohio). Group 2 contains sequences from specimens originating
from Canada (Ontario, Québec), Israel, and the United States (California, Connecticut, Florida, Illinois, Kentucky,
Mississippi, Ohio).
Adult specimens represented by sequences in Group 1 (Figs. 10–16) are primarily brown with a variably ex-
pressed interfascial spot that ranges in color from white to bronze. The paired costal strigulae on the distal one-half
of the wing are whitish and usually inconspicuous (except for strigula 9) in most individuals. The associated gray
striae extend toward the termen and are usually separated by lines of orange-brown scales. The male genitalia (Fig.
19) have socii that are long and fingerlike with lateral margins that are nearly parallel. In the female genitalia (Figs.
24–26), the sterigma is elongate and rectangular. Overall, the specimens in Group 1 are consistent with the type of
E. strenuana (Fig. 10). Adult specimens represented by sequences in Group 2 (Figs. 2–9) are primarily gray to dark
gray. The interfascial spot, when expressed, is pale gray. The white costal strigulae are usually well expressed and
more prominent than in Group 1, and the orange-brown lines between the striae are absent. The male genitalia (Figs.
17–18) have socii that are generally shorter than in Group 1, and in some specimens the socii are nearly triangular.
TAXONOMY OF RAGWEED BORER Zootaxa 4729 (3) © 2020 Magnolia Press · 351
In the females of Group 2 (Figs. 20–23), the sterigma is ovate and not as elongate as in Group 1. The specimens in
Group 2 are consistent with the type of E. minutana (Fig. 2).
FIGURE 1. Maximum likelihood tree of DNA barcode data analyzed using the GTR + gamma nucleotide substitution model.
GILLIGAN ET AL.
352 · Zootaxa 4729 (3) © 2020 Magnolia Press
Based on the DNA data and differences in morphology, we believe that E. strenuana can be reliably separated
from E. minutana. Wing coloration and the shape of the female sterigma are consistently different between the two
species. Epiblema strenuana is brown with most costal strigulae inconspicuous and orange-brown scales near the
apex of the forewing. Epiblema minutana is gray to dark gray with conspicuous white costal strigulae and a lack of
orange-brown scales on the forewing. The female sterigma of E. strenuana is more elongate and rectangular than
in E. minutana, where the sterigma is often ovate. There are some female specimens of E. minutana in which the
sterigma is somewhat elongate, but the ostium is never twice as long as it is wide. In males of E. strenuana, the socii
are long and fingerlike with parallel sides. In E. minutana, the socii can vary from fingerlike with parallel sides to
short and triangular. In general, it appears that the male socii are less reliable than the female sterigma for separating
the two species compared to the female sterigma. In all cases, genitalia characters should be combined with wing
coloration to arrive at a final determination.
Other characters suggested by previous authors (size, female signa size and shape, etc.) are too variable to
differentiate E. strenuana and E. minutana. Forewing length overlaps substantially between the two species (E.
strenuana FWL: 4.0–9.0 mm; E. minutana FWL: 4.3–7.9 mm), although on average E. strenuana is slightly larger
(mean FWL: 7.1 mm vs. E. minutana mean FWL: 6.0 mm). This size range is too close to separate any individual
specimen, and we have observed large E. minutana collected in similar locations with small E. strenuana. Other
characters, such as the female signa, also vary greatly in shape and size, and there is no consistent pattern to reliably
separate the two species.
Although our analysis of DNA barcode data resulted in two clades representing two species, there is a substan-
tial amount of variation in the E. minutana group. Sequences representing specimens from Florida and California
clustered somewhat separately from the rest of the E. minutana sequences, hinting at the possibility that these se-
quences could represent a different taxon. We were not able to discern any consistent morphological differences in
these specimens from other specimens of E. minutana, and thus assume these are simply population-level genetic
differences. In the future, it is possible that more extensive DNA-based studies could reveal that the E. minutana
clade represents a species complex; however, we have no current evidence to support this conclusion.
It is evident from this study that the species previously identified as E. strenuana in Israel (e.g., Yaacoby and
Seplyarsky, 2011) is actually E. minutana. While detailed host range tests have been conducted with the E. strenu-
ana populations released in Australia and China, the host range of E. minutana remains to be clarified. Interestingly,
in his paper on the host specificity of E. strenuana, McClay (1987) stated that E. minutana attacks A. confertiflora
in the native range in Mexico, but that “the inclusion or exclusion of E. minutana does not affect the recorded host
range of E. strenuana.” Elucidating the host specificity of the population recently established in Israel is of par-
ticular relevance, both with regard to potential non-target risks and potential benefits. Israel’s native flora is rich in
asteraceous species, and since the host range of E. minutana has not been studied, non-target attack of native species
cannot be entirely excluded. In terms of the potential beneficial effects, several alien Asteraceae species are invasive
in Israel, including Xanthium spp., Verbesina enceloides Cav., P. hysterophorus and several Ambrosia spp. (Danin,
2000). Until now, E. minutana in Israel has only been reported from A. confertiflora and A. tenuifolia (Yaacoby and
Seplyarsky, 2011). It is of high economic and ecological interest whether E. minutana also attacks other asteraceous
weeds, especially P. hysterophorus since this is a famously aggressive invasive weed (Adkins and Shabbir, 2014).
In case E. minutana does not attack P. hysterophorus in Israel, it would be sensible to search for other biological
control agents.
Species redescriptions
Epiblema strenuana (Walker, 1863)
(Figs. 10–16, 19, 24–26)
Grapholita strenuana Walker 1863:383.
Grapholita exvagana Walker 1863:383.
Steganoptycha flavocellana Clemens 1865:238.
Grapholita subversana Zeller 1875:318.
Paedisca strenuana: Walsingham 1879:52; Fernald 1882:40; Walsingham 1884:140.
Eucosma strenuana: Fernald 1903:458; Barnes and McDunnough 1917:170.
TAXONOMY OF RAGWEED BORER Zootaxa 4729 (3) © 2020 Magnolia Press · 353
Epiblema strenuana: Heinrich 1923:140, figs. 257, 258; McDunnough 1939:48; Darlington 1947:95; Miller
1972:214; Powell 1983:35; Miller and Pogue 1984:227; Miller 1987:56; Brown 2005:286; Gilligan et al.
2008:121; Horak 2008:310; Powell and Opler 2009:135; Pohl et al. 2018:151.
FIGURES 2–16. Adults. 2–9, E. minutana (2, New Jersey, lectotype; 3, Mississippi, DJW8714; 4, California, DJW8655; 5,
Kentucky, TONAB101-09; 6, Ohio, USNM152255; 7, Ohio, DJW8712; 8, Florida, DJW8739; 9, California, DJW8666). 10–16,
E. strenuana (10, North America, lectotype; 11, Alabama, DJW8703; 12, Texas, DJW8667; 13, Ohio, USNM152288; 14, Ala-
bama, DJW8704; 15, New Mexico, USNM152289; 16, California, DJW8683).
GILLIGAN ET AL.
354 · Zootaxa 4729 (3) © 2020 Magnolia Press
Types. Grapholita strenuana. Lectotype (designated by Miller and Pogue 1984) (Fig. 10). ♂, North America, Carter
Collection, BMNH(E) 819923, slide 5737, BMNH. Grapholita exvagana. Lectotype (designated by Miller and
Pogue 1984). North America, Carter Collection, BMNH(E) 819924, BMNH [hindwings and abdomen missing].
Steganoptycha flavocellana. Lectotype (designated by Darlington 1947). ♂, Type No. 7214, ANSP [abdomen miss-
ing]. Grapholita subversana. Syntypes? Texas, Boll, MCZ [Brown 2005 lists these types as lost].
Both G. strenuana and G. exvagana seem to have been described from specimens with a moderately well-
expressed white interfascial spot; Miller and Pogue (1984) designated the same specimens that N. S. Obraztsov
provisionally selected as lectotypes. The number of specimens supporting the description of S. flavocellana is
unknown. Darlington (1947) attributed the lectotype designation to Heinrich (1923), but Heinrich did not provide
enough information to designate a single specimen. Miller’s (1973) image of S. flavocellana shows the interfascial
spot to be obsolete. Zeller (1875) mentioned three or five syntypes in his description: “Texas (Boll). Massachusetts
at Beverly (Burgess) where two ♀ on 27 June and 3 July were caught. One ♂, one ♀ in Museum Cambridge, one ♀
in my collection.” Regardless of the exact number, Miller and Hodges (1990) did not report any types in the MCZ
and Brown (2005) listed the types as lost. All of the above synonymies date to Fernald (1882).
Redescription. Epiblema strenuana is a brownish to grayish species of variable size (FWL: 4.0–9.0 mm, mean
= 7.1) and average forewing geometry (AR = 2.80). The interfascial spot, which extends from the inner margin to
the radius, varies from whitish (Figs. 10, 15–16) to shades of bronze or gray (Figs. 11–14), in the latter case be-
ing weakly distinguishable from the subbasal and median fasciae by its lack of white-tipped scales. Its proximal
margin is often indicated by a thin line of pale scales (e.g., Fig. 14). The ocellus is white and conspicuous, with a
central black longitudinal dash, a black mark on the costal margin, a narrow gray band on the proximal margin, and
a black line along the basal edge of the gray band, the last often fragmented into two or three segments. The paired
costal strigulae on the distal one-half of the wing are white to gray, usually inconspicuous (except for strigula 9),
with associated gray striae extending toward the termen, the last usually separated by lines of orange-brown scales.
The specimen in Fig. 16 is representative of a few specimens from southern California that have unusually well
expressed costal strigulae.
The male genitalia (Fig. 19) are distinguished by long fingerlike socii, whose lateral margins are nearly paral-
lel. In females, the sterigma (Figs. 24–26) is rectangular and elongate (length about 2 times ostium diameter), the
posterior margin of sternum 7 is semicircular and diverges laterally from the sterigma, and the ductus bursae has a
twist-like sclerotized contortion near the juncture with the ductus seminalis.
Remarks. Heinrich (1923) stated that the larva is a stem borer on Ambrosia artimisiifolia L. (annual ragweed)
without providing the source of that information. Stegmaier (1971) reported rearing Florida specimens from larvae
feeding in fusiform galls in the lateral branches of A. artimisiifolia. He also reported rearing a similar but unknown
species of Epiblema, later determined by Miller and Pogue (1984) as E. minutana, from larvae boring in stems of
A. artimisiifolia. Other larval hosts have been mentioned in the literature, including Parthenium hysterophorus L.
(Santa Maria feverfew) (McClay 1987), Xanthium (cocklebur) (Miller 1987; Powell and Opler 2009), and Cheno-
podium (goosefoot) (Miller 1987), but these records need to be verified. Epiblema strenuana has been used as a
biological control agent for a variety of invasive weeds; those species are listed elsewhere in this paper.
This species is broadly distributed over the North American continent. We suspect the distribution of the moth
mimics that of its hosts, Ambrosia spp. Xanthium spp., and P. hysterophorus (Hilgendorf and Goeden 1983; Mc-
Clay 1987). Of course, many of the literature records are uncertain due to the long-standing confusion regarding
E. strenuana and E. minutana. We examined specimens from 14 states in the region extending from Minnesota
to Texas, west to Colorado and New Mexico, east to Maryland and Florida, and several specimens from southern
California. In the Midwest, E. strenuana has two primary flights, one in late June, and the other from mid-August
to mid-September.
Epiblema minutana (Kearfott, 1905), revised status
(Figs. 2–9, 17–18, 20–23)
Eucosma minutana Kearfott 1905:356; Barnes and McDunnough 1917:170.
Epiblema minutana: Blanchard 1979:179; Miller and Pogue 1984:227.
Eucosma antaxia Meyrick 1920:344, unnecessary replacement name for minutana.
Epiblema strenuana (not Walker): Heinrich 1923:140; McDunnough 1939:48; Powell 1983:35; Miller 1987:56; Brown
2005:286; Gilligan et al. 2008:121; Pohl et al. 2018:151, senior synonym of E. minutana.
TAXONOMY OF RAGWEED BORER Zootaxa 4729 (3) © 2020 Magnolia Press · 355
FIGURES 17–26. Genitalia. 17–18, E. minutana (17, Ohio, TMG782; 18, Ohio, USNM152256). 19, E. strenuana (Iowa,
USNM152286). 20–23, E. minutana (20, Kentucky, TMG781; 21, New Mexico, USNM152260; 22, Kansas, USNM152258; 23,
Israel, TMG784). 24–26, E. strenuana (24, TMG778; 25, Kansas, USNM152287; 26, Ohio, USNM152288).
GILLIGAN ET AL.
356 · Zootaxa 4729 (3) © 2020 Magnolia Press
Lectotype (designated by Blanchard 1979). ♂, New Jersey, Essex County, Montclair, W. D. Kearfott, July 1908,
slide 24505, USNM.
Kearfott (1905) mentioned a series of about 40 specimens from Tryon, North Carolina; Cincinnati, Ohio; New
Brighton, Pennsylvania; Plummers Island, Maryland; Belvidere, Illinois; Smith County, Tennessee; Anglesea, New
Jersey; and Essex County Park, New Jersey. Klots (1942) stated that Heinrich (1923) had designated a lectotype
from Essex County Park, New Jersey but disagreed with Heinrich’s statement that the depository was the AMNH.
Blanchard (1979) settled the matter by formally designating the lectotype listed above in the USNM.
Redescription. Epiblema minutana is a dark gray species that lacks any subcostal orange-brown coloration
near the apex of the forewing. In size it varies (FWL: 4.3–7.9 mm) much like E. strenuana (FWL: 4.0–9.0 mm)
but on average it is somewhat smaller than the latter species (mean FWL = 6.0 vs. 7.1 mm). Previous authors have
noted, and we concur, that the forewing is slightly narrower in E. minutana than in E. strenuana (AR = 3.19 vs.
2.80). The interfascial spot is often present as a paler shade of gray (Figs. 5–8), but in some individuals it is barely
discernable (Figs. 2–4). The ocellus resembles that of E. strenuana, but the white costal strigulae are usually more
prominent than in the latter species.
Epiblema minutana is similar to E. strenuana in genitalia but differs from the latter species in the following
respects: the socii (Figs. 17–18) are shorter and sometimes triangular (tapering from a broad base to a narrowly
rounded apex vs. consistently fingerlike with parallel lateral margins), and the sterigma (Figs. 20–23) is ovate in-
stead of rectangular, with length-ostium diameter = 1.56 vs. 1.95. Shape of the socii can vary and appear similar to
those in E. strenuana. Genitalic characters should be used in combination with wing coloration to make a species-
level identification.
Remarks. The typical phenotype of E. minutana (Figs. 2–8) is broadly distributed in eastern United States and
is also found in central California. In the East, the larval host is presumed to be Ambrosia artimisiifolia L. (annual
ragweed), but the adult determinations in literature reports of reared specimens need to be checked for accuracy vis-
à-vis E. strenuana. Epiblema minutana has been reared in Mexico from field-collected larvae from A. confertiflora
(McClay 1987) and in Contra Costa County, California, by J. A. Powell from Ambrosia psilostachya DC. (Cuman
ragweed), a plant with a transcontinental distribution. The EME has numerous specimens from California with
minutana-like genitalia and pale gray forewings (Fig. 9). They are somewhat larger than typical E. minutana (mean
FWL = 6.9 vs. 6.0 mm) but are nearly identical in forewing geometry (AR = 3.18 vs. 3.19). This phenotype has been
reared from A. psilostachya and from Ambrosia chamissonis (Less.) Greene (silver bur ragweed) (Powell and Opler
2009). The range of the latter plant extends along the Pacific coast from southern California to Alaska. Powell and
Opler (2009) reported larvae causing deformities at nodes of lateral decumbent stems but not forming stem galls.
Similar specimens are represented in the phylogenetic tree (Fig. 1) from San Diego County, California. These clus-
ter with typical E. minutana but show some minor consistent differences in the sequences that could indicate they
are a separate taxon. We can find no morphological differences in these California specimens, thus we tentatively
refer them to E. minutana until a more comprehensive DNA analysis can be performed. We can confirm they are not
E. strenuana, which is also present in California, and we have examined typical specimens of E. strenuana from the
same location in San Diego County.
Acknowledgements
We thank Kunjithapatham Dhileepan, Zhongshi Zhou, and Nadav Nussbaum for rearing and sending specimens
from field-collected larvae, and John Brown (USNM), Jim Hayden (FSCA), Jerry Powell (EME), and Peter Oboys-
ki (EME) for loans of specimens used in this study. Mark Metz (USDA-ARS-SEL) provided genitalia photos of
the E. strenuana lectotype in the BMNH. Alicia Timm (Colorado State University) assisted with sequencing. Urs
Schaffner was supported by CABI with core financial support from its member countries (see http://www.cabi.
org/about-cabi/who-we-work-with/key-donors/). Benno Augustinus was supported by a scholarship from the Jean
and Bluette Nordmann foundation. Mention of trade names or commercial products in this publication is solely for
the purpose of providing specific information and does not imply recommendation or endorsement by the USDA;
USDA is an equal opportunity provider and employer.
TAXONOMY OF RAGWEED BORER Zootaxa 4729 (3) © 2020 Magnolia Press · 357
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A multiple sequence alignment program, MAFFT, has been developed. The CPU time is drastically reduced as compared with existing methods. MAFFT includes two novel techniques. (i) Homo logous regions are rapidly identified by the fast Fourier transform (FFT), in which an amino acid sequence is converted to a sequence composed of volume and polarity values of each amino acid residue. (ii) We propose a simplified scoring system that performs well for reducing CPU time and increasing the accuracy of alignments even for sequences having large insertions or extensions as well as distantly related sequences of similar length. Two different heuristics, the progressive method (FFT‐NS‐2) and the iterative refinement method (FFT‐NS‐i), are implemented in MAFFT. The performances of FFT‐NS‐2 and FFT‐NS‐i were compared with other methods by computer simulations and benchmark tests; the CPU time of FFT‐NS‐2 is drastically reduced as compared with CLUSTALW with comparable accuracy. FFT‐NS‐i is over 100 times faster than T‐COFFEE, when the number of input sequences exceeds 60, without sacrificing the accuracy.