Research Article |
Corresponding author: Erik J. van Nieukerken ( nieukerken@naturalis.nl ) Academic editor: Bernard Landry
© 2018 Erik J. van Nieukerken, Daniel Owen Gilrein, Charles S. Eiseman.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
van Nieukerken EJ, Gilrein DO, Eiseman CS (2018) Stigmella multispicata Rociene. & Stonis, an Asian leafminer on Siberian elm, now widespread in eastern North America (Lepidoptera, Nepticulidae). ZooKeys 784: 95-125. https://doi.org/10.3897/zookeys.784.27296
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Stigmella multispicata Rocienė & Stonis, 2014, previously known from the single male holotype from Primorye, Russia, is reported as a new invasive species mining leaves of Siberian elm, Ulmus pumila L., in eastern North America. Both adults and leafmines have been reported from many sites as unidentified Nepticulidae since 2010. Crucial for the identification was a match of the DNA barcode of a single larva collected on Ulmus pumila in Beijing with adults from North America. The single larva constitutes a new record for China. Stigmella multispicata is closely related to the European S. ulmivora (Fologne, 1860), feeding likewise on Ulmus, but differs in details of external morphology and genitalia, particularly in the female, where S. multispicata has a remarkable elongated narrow ovipositor, suitable for oviposition in underside hairy leaf vein axils, where all mines start. In North America S. multispicata is the only Ulmus-feeding nepticulid with green larvae. Currently the species is known from USA: Illinois, Indiana, Iowa, Maryland, Massachusetts, Minnesota, New York, Ohio, Tennessee, Wisconsin, and Canada: Ontario and Québec. In Sagaponack, on Long Island, New York, larvae have been reported to occur en masse on Siberian elms from at least two sites. The current distribution could be reconstructed thanks also to many online photographs from observation websites. The species is redescribed, with the first descriptions of female, larva, and leafmine, and compared with S. ulmivora, which is fully redescribed. The two native North American nepticulid Ulmus leafminers, S. apicialbella (Chambers, 1873) and Ectoedemia ulmella (Braun, 1912), are diagnosed and new provincial and state records are provided. A key to linear mines on Ulmus in North America is provided. We suspect that trade of live plants through nurseries played a role in the sudden spread of this invasive species.
Canada, China, DNA barcoding, invasive, key, pest species, Stigmella ulmivora , Ulmus pumila , United States
The North American insect fauna has been enriched by an influx of numerous alien species. Most invasions in temperate North America originate in Europe, far fewer in Asia (
Beginning around 2010, James Vargo found numerous specimens of an unknown Stigmella species that he had not seen before, while light collecting on his property in Indiana, USA. Material was sent to specialists Don Davis and David Wagner, neither of whom recognized the moths as belonging to a known American species. EJvN got some of these specimens when borrowing unidentified Nepticulidae from the Mississippi Entomological Museum in 2010, and also failed to name them. A near match of the DNA barcode with a larva collected in 2013 from a leafmine on Ulmus in Beijing, China, was striking, but initially regarded as coincidental.
In October 2015, DOG received a sample of green nepticulid larvae from Ms. Lee Foster in Sagaponack on Long Island, Suffolk County, New York, that were descending en masse on silk strands from Siberian elm (Ulmus pumila L.) (Figs
Online photographs of adults and leafmines of Stigmella multispicata. Identifications by E.J. van Nieukerken. All leafmines on Ulmus pumila.
Stage | State | County/City | Locality | Date | Observer | url |
---|---|---|---|---|---|---|
Canada | ||||||
1 adult * | Ontario | Toronto | Yarmouth Gardens | 26.vii.2015 | D. Beadle | https://www.inaturalist.org/observations/9482752 |
1 adult | Ontario | Toronto | Yarmouth Gardens | 18.vii.2016 | D. Beadle | https://www.inaturalist.org/observations/9542202 |
United States | ||||||
1♀ | Illinois | Cook | Skokie, Balaban House | 24.viii.2017 | John & Jane Balaban | https://bugguide.net/node/view/1439557 |
ca 8 mines | Illinois | Lisle | The Morton Arboretum | 4.x.2010 | Bruce J. Marlin | http://www.cirrusimage.com/tree_Siberian_Elm.htm |
ca. 3 young mines | Illinois | Urbana | residential area | 4.ix.2010 | John Hilty | http://www.illinoiswildflowers.info/trees/plants/sb_elm.html |
3 mines | Iowa | Shelby | south of Elk Horn | 19.x.2016 | M.J. Hatfield | https://bugguide.net/node/view/1362960 |
1♂ | Iowa | Winneshiek | 100 Acre Wood | 27.vii.2014 | M.J. Hatfield | https://bugguide.net/node/view/966519 |
1♂ ** | Iowa | Winneshiek | Plymouth Rock | 26.ix.2014 | M.J. Hatfield | https://bugguide.net/node/view/1028011 |
old mines*** | Maryland | Baltimore City | Herring Run Park | 15.x.2013 | Thomas Wilson | https://bugguide.net/node/view/906301 |
1 adult | Minnesota | Hennepin | Minneapolis | 19.viii.2013 | Bill Johnson | https://bugguide.net/node/view/813155 |
1 adult | Ohio | Pickaway | Orient | 7.viii.2012 | Gregory Raterman | https://bugguide.net/node/view/686805 |
1 adult | Tennessee | Davidson | Nashville | 25.vii.2010 | Steven Loftin | https://bugguide.net/node/view/433176 |
1 adult | Wisconsin | Dane | Cross Plains | 4.ix.2010 | Ilona L. | https://bugguide.net/node/view/451465. |
The Nepticulidae (pygmy moths) of North America were revised almost 40 years ago (
The Nepticulidae of East Asia are best known from Far East Russia, especially the Primorye region, by studies of J. Stonis (formerly R. Puplesis) and his students (
We will here redescribe Stigmella multispicata, compare it with the European S. ulmivora (Fologne, 1860) and the other North American species of Nepticulidae feeding on Ulmus, and discuss the probability of its invasion from Asia into North America.
The material of S. multispicata from the United States and Canada originates from several sources; the few adult specimens from Canada were collected during the School Malaise Trap Program (
Material of the other species discussed here mostly originates from the collections of the Naturalis Biodiversity Center, Leiden, Netherlands. The Material examined section provides only the basic locality data, all details on registration numbers, genitalia slides, collectors etc. are provided in the Suppl. material
BIN Barcode Index Number (Ratnasingham and Hebert 2013)
BOLD Barcode of Life Data Systems (http://www.barcodinglife.com/)
CSEC C.S. Eiseman Research Collection
MEM Mississippi Entomological Museum, Starkville, Mississippi, United States
For the collection of leafmines in China see van
Genitalia were prepared according to our standard procedures, usually including DNA extraction, which were described earlier in detail (van
Measurements of genitalia were obtained from digital images, using calibrated scaling in the Zeiss AxioVision software; we used a 20× objective for male genitalia and 10× or 20× for female genitalia. Capsule length was measured from vinculum to middle of uncus; valva length from tip of posterior process to ventral edge, excluding the sublateral process; phallus length was measured along the sclerotized tube, from tip, excluding any protruding vesica parts. Total bursa length includes all of the internal genitalia from cloaca to anterior edge of bursa; apophyses were measured from abdominal tip to anterior tip of apophyses. Genitalia measurements are rounded off to the nearest 5 μm. Forewing length was measured from tip of fringe to attachment on thorax, with a Zeiss SV11 stereo-microscope at a magnification of 20×. Antennal segment counts include scape and pedicel; they were counted on photographs or directly under the same stereo microscope.
Photographs of moths were made with an AxioCam MRc 5 digital camera attached to a motorized Zeiss SteREO Discovery V12, using the Module Extended Focus, Zeiss AxioVision software, to prepare a picture in full focus from a Z-stack of ca 10 to 40 individual photos. Leafmines were photographed by EJvN with an AxioCam HRc camera on a Zeiss Stemi SV11 stereo-microscope, without extended focus. Photos by CSE were taken either with a Canon EOS Rebel XSi SLR digital camera, and MP-E 65 mm macro lens (Figure
Our methodology for DNA barcoding has been described in other papers (van
Stigmella
multispicata
Rocienė & Stonis in Stonis & Rocienė, 2014: 205. Holotype ♂, Russia, Primorskiy Kray, 20 km E Ussuriysk, Gornotayezhnoe, Biological Station, 8.viii.2011, leg. A. Rocienė, genitalia slide no. AG427 (
Stigmella
multispicata
; van
In North America S. multispicata is the only Stigmella species with the combination of black frontal tuft, white collar, and single fascia. Stigmella quercipulchella (Chambers, 1882) is relatively similar, but has an additional silver patch at tornus, is slightly larger and has more strongly purple reflections across the forewings. This combination of characters is also diagnostic in East Asia, but there remains a possibility that similar species will be discovered. From the closely related European S. ulmivora it differs by the white collar (dark in ulmivora) and the entirely dark antennae (those of S. ulmivora have the distal 7–8 flagellomeres white); S. ulmivora is also slightly larger and has more antennal segments. The female of S. multispicata differs from all more or less similar species by the obvious long ovipositor, visible even without dissection.
Male genitalia differ from those of S. ulmivora in the shallowly indented uncus and the very short sublateral processes of the transtilla; the female genitalia are easily recognized by the long apophyses; the ductus spermathecae has no spines in contrast to S. ulmivora. Some species in the S. rhamnella group have superficially similar male genitalia, but they have no juxta, and the moths are externally very different.
Stigmella multispicata leafmines are characterized by the egg placement on the leaf underside in vein axils, larval exit on leaf underside, and green to blue-green larval color.
Male (Figs
Stigmella species, adult habitus. 1 S. multispicata, male, USA, Indiana,
Female (Figure
Male genitalia (Figs
Stigmella species, male genitalia in ventral view. 7, 8, 12 S. multispicata, slide EvN4511,
Female genitalia (Figs
Larva (Figs
Stigmella multispicata, immature stages and leafmines on Ulmus pumila. 19 leafmine of barcoded larva,
Host plants. Ulmus pumila L. (Ulmaceae), Siberian elm, a widespread tree in East Asia, cultivated globally in temperate climates, widely planted in North America. Vacated mines presumably representing this species were also collected in China on Ulmus macrocarpa Hance, Large-fruited elm.
Leafmine (Figs
Larva (Figs
Life history. Larvae and leafmines found in China in October; in North America larvae were observed from 15 June to mid-July and from 19 October to 6 November. Moths were found on 26 May and from 8 July throughout August to 6 September (with a peak between 10 and 15 August), a few late records from 22 and 26 September and 2 October. Moths reared from October mines emerged in the laboratory between 25 March and 19 May. The species has at least two annual generations, maybe more. Adults are frequently found at light.
(Figs
All eight barcodes belong to BINBOLD:ACP7362. All North American barcodes are 100% identical; the single Chinese one differs in 11 basepairs (1.7%). The nearest neighbor, at 6.3%, is Stigmella ulmivora (Figure
The extensive collections of Chinese microlepidoptera of Nankai University were searched in vain for this species (Li Houhun, personal communication to EvN). It is possible that specimens can be found in other collections in China, such as the Zoological Institute in Beijing.
19♂, 26♀, 3 sex undetermined, 5 larvae, mines. China: 1 larva (green, dried out, destructively extracted for DNA), China, Beijing, Beijng Botanical garden – Wofosi, E.J. van Nieukerken & S. Richter, 17.x.2013, EvN no 2013117–M, Ulmus pumila, N40.00417, E116.20419, 108 m,
Canada: 1♂,1♀ (in ethanol 96%), Ontario, Toronto, Etobicoke School of the Arts, EQP–CLL–602, Brad Schumacher, 22–28.ix.2014, GMP#05745, Malaise trap, N43.631, W79.504, 109 m, BIOUG16150–E04, BIOUG16150–E05 (
United States: 1♀, Indiana, St. Joseph Co., J. Vargo, 26.v.2010, N 41.37’46.2”–W 86.08’13.9”, [N41.62950, W86.13719] (
China: 4 tenanted mines (rearing failed), Beijing, Xiangshan, Wofosi and botanical garden, E.J. van Nieukerken & J.W. van Driel, 1.x.1984, EvN no 18–1–1K, Hills with deciduous shrub and low trees, U. macrocarpa, N39.983, E116.2, 100–500 m,
Canada (Data from BOLD, barcode identification): 1 adult, Ontario, Waterloo region, Kitchener, Crestview Public School, EQP-CLL-863, Sherrie Cochrane, 2.x.2015, GMP#08378, N43.454, W80.44, 334m, BIOUG25491–E12 (
United States (Observations, personal communications to authors): 4 larvae/mines, Indiana, St. Joseph Co., J. Vargo, 15–29.vi.2018; 120 adults, St. Joseph Co., Mishawaka, J. Vargo, 8.vii.2018, light trap; larvae descending en masse from trees, New York, Suffolk Co., Sagaponack, Ms. Lee Foster, 21.x.2015, U. pumila, N40.93, W72.28; larvae still present, same locality, 8.xi.2015; larvae, same locality, Mike Harmon, 16.vii.2016; larvae, same locality, 19.x.2016; larvae descending en masse from trees, New York, Suffolk Co., Wainscott, 3.xi.2015, Mike Harmon, U. pumila, N40.94, W72.24.
Nepticula ulmivora Fologne, 1860: 199. Syntypes, Belgium, Brussels region, reared from Ulmus, 1859, emerged 1860, Fologne [probably lost].
Stigmella
ulmivora
;
Stigmella ulmivora can be separated from S. multispicata by the slightly larger size, the dark collar, and the antennae with the terminal 7–8 flagellomeres white. In Europe and North America there are no other Stigmella species with the same combination of characters. The male genitalia are very similar to those of S. multispicata, but have a deeper indentation in the uncus, and longer and more distinct sublateral processes of the transtilla. The female differs by the blunt ovipositor and the spiny ductus spermathecae.
Leafmines differ from those of S. multispicata by the egg position not being in vein axils; in Europe mines are inseparable from those of S. ulmiphaga (Preissecker, 1942). Due to the variability of mines of S. ulmivora, they sometimes are difficult to separate from those of S. lemniscella (Zeller, 1839), from which the yellow larva emerges through the leaf upper side, not the underside as in S. ulmivora.
Male (Figure
Female (Figure
Male genitalia (Figs
Female genitalia (Figs
Larva (Figs
Host plants. Ulmus minor Mill., U. glabra Huds., Ulmus spp. (Ulmaceae). Reared specimens labeled as coming from Acer were from cocoons found on trunks of that tree; therefore this cannot be considered a host record.
Leafmine (Figs
Larva (Figure
Life history. Bivoltine, or possibly partially univoltine in northern parts of Europe. Larvae in June to early July, again in August to November. Adults recorded from May (a single April record) to early July and again in August.
Widespread throughout Europe, east to the Volga region in Russia (
We have 13 barcodes from across Europe, all belonging to BINBOLD:AAI0023, with some variation, a maximum distance for the Greek barcodes of 2.41% to the rest. The nearest neighbor, at 6.31%, is Stigmella multispicata (Figure
Adults: 25♂, 50♀. Croatia: 1♂, Krk, Kampelje, 17.viii.2001; 1♀, Krk, Mt. Hlam, loc. Branusine, 15.viii.2012. Germany: 1♀, Berlin; 1♂, Thüringen, Bad Blankenburg, Muschelkalk, 1.vii.1986; 1♀, Thüringen, Bad Blankenburg, Schwarzatal, 5.vii.1986. Italy: 1♂, Cuneo, Entracque, ca 1 km SE, Il Bosco, 16.viii.2007, la on Ulmus; 1♂, 1♀, same locality, 13.x.2008, la on Ulmus; 1♀, Latina, Monti Aurunci, 4 km NW Castelforte, 22–23.vi.1969. Netherlands: 2♂, 2♀, Gelderland, Wageningen, Ulmus, e.l. 19.v.1977; 1♀, ibidem, larva x.1989, Ulmus; 2♂, 3♀, Noord-Brabant, Breda, v.1877; 1♀, ibidem, e.l. 10.vi.1877, “acer pseudop.”; 2♂, 1♀, ibidem, e.l. 25.vi.; 1♀, 3 damaged adults, ibidem, v.1878; 1♀, Noord-Holland, Amsterdam, 2.viii.1937; 1♂, Noord-Holland, Amsterdam, Koloniaal instituut, 7.viii.1937; 1♀, Noord-Holland, Amsterdam, Ulmus, e.p. 30.vi.1929; 1♀, ibidem, Ulmus e.l. 27.iv.1942; 5♀, ibidem, Ulmus e.l. 29.vii–2.viii.1943; 1♀, Noord-Holland, Amsterdam N.W., Ulmus, 16.viii.1942; 1♂, 4♀, ibidem, Ulmus e.l. 2–14.viii.1947; 1♀, ibidem, Ulmus e.l. 6.vi.1948; 1♀, ibidem, Ulmus e.l. 11.vi.1948; 1♀, Noord-Holland, Bussum, 16.iv.1934; 1♂, Noord-Holland, Castricum, 15.viii.1979, Ulmus e.l. 13.vi.1980; 6♂, 9♀, Noord-Holland, Hilversum, Ulmus e.l. 4–24.vi.1943; 4♀, ibidem, Ulmus e.l. 17.v.–6.vi.1945; 1♀, Noord-Holland, Overveen, 7.vi.1929; 1♂, ibidem, 1.vii.1929; 2♀, Zuid-Holland, Den Haag, Ulmus e.l. 9.v–10.vi.1865; 1♀, Zuid-Holland, s Gravenhage, 29.v; 1♀, Zuid-Holland, Lexmond, 3.viii.1999; 1♂, Zuid-Holland, Rottm. [Rotterdam], e.p. 22.vi.1901; 1♂, ibidem, e.l. 24.vi.1864; 1♂, ibidem, e.l. 13.vii. 1870; 1♂, ibidem, 21.vi.1877; 1♀, ibidem, pupa in iv, e.p. 21.vii.1879; 1♀, ibidem, 27.v.1877. Poland: 1♂, Silesia, Wroclaw (Breslau), e.l. iii.1882.
Leafmines and larvae. When no hostplant is given, read Ulmus sp. – Czech Republic: 1 mine, Moravia, Lednice, 3 km SW, forest near lake, 3.x.1992. France: 4 larvae, vacated mines, Alpes-Maritimes, Saorge, 0.8 km SW, vallée de Roya, 9.x.2008, U. minor; 1 vacated mine, Alpes-Maritimes, Tende, ca 1 km S, E. slope, 10.x.2008, U. glabra; mines, Bouches-du-Rhône, Aix-en-Provence, Parc Jourdan, 12–16.x.1983; several vacated mines, Cher, Villeneuve-sur-Cher, 30.vii.2009, U. minor; vacated mines, Drôme, Beaurières, 4 km W: Marais des Boulignons, 21.viii.2002; 1 vacated mine, Eure, Le Marais Vernier, la Vallée, 5.x.2017; 2 vacated mines, Finistère, Presqu’île de Crozon, ca 4 km E Crozon, l’Aber, 12.vii.2006; 1 vacated mine, Haut-Rhin, Colmar, 3 km SW, Le Neuland, 26.ix.2002; 1 larva, 4 mines, Haut-Rhin, Lapoutroie, La Bohle, 21.x.2002, U. glabra; 3 vacated mines, Indre-et-Loire, Huismes, N of Contebault, along C17, 8.x.2017; several vacated mines, Lozère, Marjoab, 2.5 km SW Meyrueis, 22.vii.2009, U. minor; 3 vacated mines, Lozère, Barre-des-Cévennes, 26.vii.2009, U. minor; vacated mines, Pyrénées-Orientales, Port-Vendres, near railway station, 28.vii.1982. Germany: 1 vacated mine, Brandenburg, Erkner, 9–11.ix.2007; several vacated mines, Saarland, Neunkirchen, Zoo, 30.ix.2004; 1 vacated mine, Sachsen-Anhalt, Dornburg, 2 km S, along Elbe, 19.vii.2014. Greece: 2 larvae, many mines, Akhaia, Strofilia, S Kalogria, 4.xi.2011, U. minor; 6 larvae, several mines, Ilía, Olympia, archeological site, 5.xi.2011, U. minor. Italy: 1 vacated mine, Bolzano, Vinschgau, Prad an Stilfser Joch, Suldenbach banks, 27.vii.2005; 1 larva, many mines, Cuneo, Entracque, ca 1 km SE, Il Bosco, 16.viii.2007; several mines, Cuneo, Entracque, ca 1 km SE, Il Bosco, 13.x.2008; 3 vacated mines, Roma, Trevignano Romano, 17.ix.2005. Monaco: 3 vacated mines, Monaco Ville, E slope of Palais Principier, 9.viii.2007. Netherlands: mines, Gelderland, Winterswijk, Bekendelle, along Slinge, 1.x.1979; 1 larva, mines, Gelderland, Nijmegen, Winkelsteeg, 11.x.2008; mines, Limburg, Eys, railway near Piepert, 11.ix.1979; mines, Limburg, Thorn, klooster Bethanien, 24.ix.1979; mines, Limburg, Gulpen, NW, holle weg, 8.x.1979; 1 mine, Limburg, Thorn: Baarstraat, 3.x.1988; mines, Noord-Holland, Castricum, hedge along road, 15.viii.1979; mines, Noord-Holland, Castricum, hedge along road, 15.viii.1979; mines, Noord-Holland, Amstelveen, Beneluxbaan, median reserve, 21.ix.1979; several vacated mines, Overijssel, Weerribben, Ossenzijl, Venebosch, 27.viii.2011; several vacated mines, Zeeland, Middelburg N., Brigdamseweg, 2.viii.2009; 1 larva, 1 mine, Zuid-Holland, Den Haag, Waalsdorpervlakte, 7.x.2007; mines, Zuid-Holland, Leiden W, experimental garden University, 5.vii.1979; mines, ibidem, 5.ix.1979; mines, Zuid-Holland, Wassenaar, Meijendel, near Kijfhoek, 18.ix.1979; 1 larva, Zuid-Holland, Oegstgeest, Rhijngeest, 23.ix.1997. Portugal: 1 mine, Tras-os-Montes, PN Montesinho, Salgueiros, Vallone das Furnas, 8 km N Vinhais, 30.vii.2001. Romania: a few vacated mines, Brasov, Brașov, Mt. Tâmpa, 2.viii.2011. Sweden: several vacated mines, Bohuslan, Svenneby, Valön Nature Reserve, 7.viii.2008.
Previously only two Nepticulidae were known to feed on Ulmus in North America: Stigmella apicialbella (Chambers, 1873) and Ectoedemia ulmella (Braun, 1912). This is a much poorer fauna than the seven European species (van
Identification of the North American Nepticulidae mines and adults reared from Ulmus is straightforward. For convenience we provide a key that distinguishes these from other insects that form partially or entirely linear mines. Primary blotch mines on elm are formed by additional species of Lepidoptera (Coleophoridae: Coleophora; Gracillariidae: Cameraria, Phyllonorycter), Coleoptera (Buprestidae: Brachys; possibly also Curculionidae: Tachygonus), and Hymenoptera (Tenthredinidae: Fenusa). For a complete key, see
1 | Linear-blotch mine formed in spring; egg inserted in the leaf | 2 |
– | Linear or linear-blotch mine formed in summer or fall; egg deposited on the leaf surface | 3 |
2 | Mine originating at a scar on the underside of the leaf midrib; frass forming a central line in the linear portion; larva with a head capsule, pupating in a globular cocoon within the mine | Orchestes spp. (Coleoptera: Curculionidae) |
– | Mine typically originating near the leaf margin, not associated with a scar; frass indistinct in the linear portion; larva without a head capsule, exiting the mine to pupate | Agromyza aristata Malloch, 1915 (Diptera: Agromyzidae) |
3 | Mine approx. 2 cm long and less than 1 mm wide, mostly following the midrib and one or two lateral veins; frass filling the width of the mine except for the terminal several mm, in which no frass is deposited; larva emerging to feed externally in patches on the lower leaf surface | Bucculatrix (Lepidoptera: Bucculatricidae) |
Note: Bucculatrix eclecta Braun, 1963 has been reared from elm but no details of the mine were recorded ( |
||
– | Mine longer than 2 cm and eventually more than 1 mm wide, with extended portions that do not follow veins; frass at least initially forming a narrow central line; larva feeding as a miner throughout its development | 4 |
4 | Mine distinctly linear throughout its length; egg usually on the lower leaf surface; cocoon never spun within the mine | 5 |
– | Mine contorted to form a blotch in the later portion, although parts of the mine may be linear; egg often on the upper leaf surface; cocoon of overwintering generation sometimes spun within the mine (Figs |
Ectoedemia ulmella (Lepidoptera: Nepticulidae) |
5 | Egg deposited on either leaf surface, may be next to a vein but not in an axil; larva yellow, exiting through the upper epidermis; on native elms (Figs |
Stigmella apicialbella |
– | Egg deposited on the lower leaf surface, in a vein axil and beneath the trichomes; larva green, exiting through the lower epidermis; on Siberian elm (Figs |
Stigmella multispicata |
Nepticula apicialbella Chambers, 1873: 127.
Stigmella
apicialbella
:
Stigmella apicialbella (Figure
Host plants. Ulmus americana L., U. alata Michx., U. rubra Muhl. (= fulva Michx.), U. thomasii Sarg. (= racemosa D. Thomas), Ulmus spp. (Ulmaceae) (
Leafmine (Figs
Stigmella apicialbella, leafmines. 36 Vacated mine, Canada, Québec, Brome-Missisquoi,
Larva (Figure
Life history. Bivoltine, or possibly trivoltine (
Widespread in Eastern North America, positive records from: Canada: New Brunswick, Ontario (BOLD: BIOUG33718-A12), Quebec (van
We have three DNA barcodes, all with BINBOLD: ACG9146 (Figure
The leafmines of this species are remarkably variable. Since we have not seen any adults or DNA barcodes yet from the southernmost states, the possibility that some of these mines represent other taxa cannot be excluded.
Canada: 1 larva, several mines, Québec, Brome-Missisquoi, St Armand, Étang Streit, 7.ix.2015, Ulmus americana; 1♀, Québec, Gatineau, Aylmer, 18 rue Washington, 19.v.1998. United States: several vacated mines, Alabama, Monroe Co., Haines Island Park, along Alabama River, 12.x.2010, Ulmus; several vacated mines, Connecticut, Litchfield Co., Canaan, Page Road near Falls Village, 11.ix.2011, U. americana; 8 vacated mines, Georgia, Murray Co., Chattahoochee Nat. Forest, E of Chatsworth, GA rd 52, 14.x.2010, U. alata; 1♂, Indiana, St. Joseph Co., 25.v.2010; 1♂, ibidem, 13.viii.2010; 3♂, ibidem, 15.viii.2010; 1♂, Kentucky [Kenton Co., Covington], Lectotype; 1 adult, Massachusetts, Hampshire Co., Northampton, Northampton Bikeway west of King St., 13.ix.2013, Ulmus, emerged 22.v.2014; 3 vacated mines, Mississippi, Oktibbeha Co., Black Prairie Reserve, nr 16th Section Rd, 6.x.2010, U. alata; 1 vacated mine, Mississippi, Winston Co., Tombigbee Nat. Forest, Noxubee Hills trailhead, 7.x.2010, U. alata; 2 vacated mines, New York, Essex Co, S Wilmington, W branch Ausable river, 13.ix.2011, U. americana; 1 larva, mines, Tennessee, Obion Co., Reelfoot Lake, 17.xi.2012, Ulmus; 1 larva, 2 mines, Vermont, Addison Co., Addison, Dead Creek WMA, 16.ix.2011, U. americana; 1 vacated mine, Vermont, Chittenden Co., Burlington, Colchester Bog, 5.ix.2015, U. americana.
Online photographs: Canada: vacated mine, New Brunswick, York Co., Fredericton, 28.viii.2015, Christopher Adam, https://bugguide.net/node/view/1162297, United States: 1 adult, Illinois, Cook Co., Glencoe, 22.v.2017, James F. Steffen, https://bugguide.net/node/view/1373817; mine with larva, North Carolina, Durham Co., Durham, Pelham Road, 25.vi.2016, U. alata, Tracy S. Feldman, https://bugguide.net/node/view/1247382, plus many records of vacated mines from NC.
Nepticula ulmella Braun, 1912: 87.
Ectoedemia
ulmella
:
Ectoedemia ulmella (Figure
Host plants. Ulmus americana L., U. alata Michx., U. rubra Muhl. (= fulva Michx.), U. thomasii Sarg. (= racemosa D. Thomas) (Ulmaceae) (
Leafmine (Figs
Ectoedemia ulmella, leafmines. 40, 41 Vacated mines, Canada, Québec, Brome-Missisquoi,
Larva. Pale yellowish white, feeding with venter upwards, ganglia usually obvious; head capsule translucent brown. Larva spinning brown cocoon inside mine or on debris.
Life history. Larvae found from July to early October, possibly in two generations, but it is also possible that this represents one extended generation. Adults recorded from May to August. From larvae collected in August, the adults emerged the following year.
Widespread in Eastern North America, positive records from: Canada: New Brunswick*, Ontario, Quebec, USA: Alabama*, Florida*, Kentucky, Maine, Maryland*, Massachusetts*, Mississippi*, New York, North Carolina*, Ohio, Pennsylvania, Tennessee*, Vermont* (
In BOLD there are two specimens from Texas with a distant but related DNA barcode (BOLD:ABX4315); we have not yet checked whether these also belong to E. ulmella.
Canada: 2♂, 1♀, 1 leafmine, Ontario, La Passe, e.l. 22.ii–26.iii.1971, Ulmus americana; 4 leafmines, Ontario, Ottawa, 28.vii–7.viii.1955, U. americana; 1♀, 5 leafmines, Ontario, Overbrook, 22.vii–7.viii.1955, U. americana; 2 larvae, several mines, Québec, Brome-Missisquoi, St Armand, Étang Streit, 7.ix.2015, U. americana; 4 vacated mines, Québec, Gatineau, Aylmer, Deschênes, Ottawa rivershore, 12.ix.2015, U. rubra; 1♂, Québec, Gatineau, Aylmer, 11.vi.1989; 1♀, ibidem, 7.vii.1989; 1♂, Québec, Gatineau, Aylmer, 48 rue Notre-Dame, 1.viii.1997; 1♂, 1♀, Québec, Gatineau, Aylmer, 18 rue Washington, 21–22.vi.1999; 3♂, 4♀, 11 leafmines, Québec, Kingsmere, 10–11.ix.1955, e.l. 12.v–17.vii.1956, U. rubra; 5 leafmines, Québec, Kingsmere, 1971, U. americana; 4 leafmines, Québec, Quyon, 1969, U. americana. United States: several vacated mines, Alabama, Monroe Co., Haines Island Park, along Alabama River, 12.x.2010, Ulmus; several mines, Florida, Volusia Co., Lake Woodruff NWR, Mud Lake Road, 24.ix.2016, U. americana; 1♀, Maryland, Calvert Co., Calvert, Scientists Cliffs, 2179 Bluebell Road, 3.viii.2007; vacated mines, Massachusetts, Hampshire Co., Northampton, Northampton Bikeway west of King St., 13.ix.2013, Ulmus; several vacated mines, Mississippi, Oktibbeha Co., Black Prairie Reserve, nr 16th Section Rd, 6.x.2010, U. alata; 1 larva, several mines, New York, Essex Co., S Wilmington, W branch Ausable river, 13.ix.2011, U. americana; several mines, New York, Essex Co, Wilsboro, Noblewood Park, 14.ix.2011, U. americana; 1♂, New York, Tompkins Co., Cornell Univ., e.l. 14.viii.1994, Ulmus; 3 vacated mines, North Carolina, Haywood Co., NP Great Smoky Mts, Big Creek area, 28.ix.2010, U. alata; 3 larvae, several mines, Tennessee, Blount Co., NP Great Smoky Mts, Rich Mountain Gap, 2.x.2010, U. americana; 1♂, 2♀, several mines, Tennessee, Blount Co., Townsend, Laurel Valley, 3.x.2010, e.l. 11–19.iv.2011, U. americana; 1 vacated mine, Vermont, Addison Co., Addison, Dead Creek WMA, 16.ix.2011, U. americana; 2 vacated mines, Vermont, Chittenden Co., Burlington, Colchester Bog, C. Eiseman & J. Blyth, 5.ix.2015, U. americana.
Online photographs: Canada: vacated mines, New Brunswick, York Co., Fredericton (Lincoln Trail), 9.ix.2014, Christopher Adam, https://bugguide.net/node/view/1042642.
Morphology and DNA barcoding show clearly that the North American and Asian populations of Stigmella multispicata are conspecific, suggesting a recent invasion by this species. We think that the invasion must have been from Asia to North America and not the other way around. Although the North American fauna is not yet completely known, a species that is now so abundant and widespread would have been hard to miss by earlier collectors, but not a single older specimen has been found in collections. Also its occurrence on the introduced Siberian elm and (so far) absence from native elm species speaks in favor of an Asian alien. The close relationship between S. multispicata and the western Palearctic S. ulmivora in the Palearctic S. ulmivora species group (van
The date of introduction is difficult to assess. Our oldest North American records are from 2010, but since those already are numerous, the species must have been well established several years before that. Since nepticulids are able to spin their cocoons on many substrates, including tree trunks, branches or other objects, we assume that an introduction of larvae or pupae inside cocoons with plants of Siberian elm, or even another plant or object, is most likely; transport of insect invaders with live plant material is considered a major pathway for exotic herbivores (
There is a parallel with another invasive Asian leafminer, the weevil Orchestes steppensis Korotyaev, 2016 (
The Siberian elm was introduced in the United States around 1860 and is widely planted for windbreaks and lumber, and now itself an invasive species, particularly in pastures, roadsides and prairies throughout the Midwest and Great Plains regions (
At the time of writing, Stigmella multispicata already is widespread in eastern North America, from eastern New York to western Iowa, and from Minnesota and Québec to Tennessee. Although the collected material gives a good insight already, online observation websites have been very helpful in providing a quick survey of the distribution, as this source alone was responsible for five of the state records. So far, S. multispicata does not appear to have risen to the status of a damaging pest. Although Siberian elm is no longer widely planted as an amenity tree, many specimens remain in urban and residential areas, where the descending larvae and aesthetic damage could be a concern. At this point the damage by S. multispicata is local, and probably not yet a great problem. In most places, the mines of O. steppensis outnumber those of S. multispicata. We advise to follow a prudent course and monitor both species simultaneously to document their spread and impact.
We acknowledge many people for sharing information and/or material: James Vargo for information on the material collected at his property, and donating this to major collections; Steven Passoa for the donation of material collected by David Shetlar to EvN; Lee Foster and Mike Harmon for informing DOG on the abundance of larvae and mines in Sagaponack, NY and sending material (Lee Foster); Richard Brown (MEM), Don R. Davis (
Li Houhun (Nankai University, Tianjin, China) kindly scanned his collections for this species. Natalia Kirichenko pointed us to the recent work on Orchestes steppensis. We are grateful to the late Liu Youqiao and Chris Wilkinson for organizing the 1984 collecting trip to China by EJvN and Li Houhun for hosting EJvN in 2013.
Jean-François Landry, Kai Berggren, Marko Mutanen and BOLD staff are acknowledged for the use of DNA barcodes from their projects. Camiel Doorenweerd and Frank Stokvis are thanked for molecular analyses and Sjaak Koster for genitalia preparations.
Reviewers David Wagner, Hector Vargas, and subject editor Bernard Landry are acknowledged for constructive remarks on the manuscript.
Specimen data of Stigmella multispicata and other Ulmus mining Nepticulidae