Research Article |
Corresponding author: Erik J. van Nieukerken ( nieukerken@naturalis.nl ) Academic editor: Kevin Keegan
© 2024 Erik J. van Nieukerken, Donald R. Davis, Steven V. Swain, Marc E. Epstein.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
van Nieukerken EJ, Davis DR, Swain SV, Epstein ME (2024) A new North American species of Etainia (Lepidoptera, Nepticulidae), feeding on Arbutus and Arctostaphylos species (Ericaceae). ZooKeys 1193: 195-218. https://doi.org/10.3897/zookeys.1193.116982
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Etainia thoraceleuca van Nieukerken, Epstein & Davis, sp. nov. is the second native American species of Etainia Beirne, 1945, and the second known Etainia species feeding on Ericaceae. The species is known from light-collected adults in the USA (California, Arizona) and Canada (Ontario). These were linked via DNA barcodes to larvae that make short leafmines on Arbutus and Arctostaphylos species, then continue feeding in stems and branches, causing damage in nurseries and planted trees in Sonoma and Marin Counties, California. The holotype was accidentally reared from Arbutus arizonica, without observing the damage. Life history and damage are described in detail. Damage in Arctostaphylos uva-ursi found in Washington State probably belongs to E. thoraceleuca, which is a sister species to the European E. albibimaculella (Larsen, 1927).
Arizona, California, Canada, insect damage, leafmines, stem mines, taxonomy, United States
Trees of the genus Arbutus are popular as planted trees for landscaping and gardening in western North America; this applies both to the native Pacific madrone (A. menziesii Pursh) as well as to the European Strawberry tree (A. unedo L.) and the cultivar Arbutus ‘Marina’, which is of obscure hybrid origin, probably from European stock (
The Nepticulidae are a medium–large family of very small moths, of which the majority make leafmines as larvae. Globally around 1000 species are known, and 97 named species occur in North America, but many are still unnamed (
The genus Etainia Beirne, 1945 is one of the smaller nepticulid genera with only 17 named species from Asia, Europe, Africa, and North America (
The European E. albibimaculella (Larsen, 1927) feeds on bearberry (or kinnikinnick), Arctostaphylos uva-ursi (L.) Spreng., and makes mines that start in the leaf but then immediately enter the shoots (
Adults in the genus Etainia can be best recognized by the long apodemes on the dorsal surface of the valvae in the male genitalia (e.g. Fig.
We here describe the new species and compare it with congeners and other similar North American species. The other two North American species were previously treated by
We list here material without coordinates, more detailed specimen data are provided in GBIF dataset https://doi.org/10.15468/espa8k.
BIN Barcode Index Number (
BOLD Barcode of Life Data Systems (http://www.barcodinglife.com/);
Adults were usually collected at light by various collectors. The holotype was reared accidentally. SVS collected adults by setting five-gallon Arbutus ‘Marina’ (bush) trap plants out nearby infected trees from 2900 Wild Turkey Run, in the Bennett Valley area south of Santa Rosa, California. Once trap plants showed symptoms of infestation, they were transported back to a holding area, where the plants had plastic funnels constructed around their bases (0.013 mm clear polycarbonate sheeting cut and glued into a 68 cm tall funnel, with a top opening of 46 cm and a bottom opening of 25 cm). Nets measuring 175 cm × 71 cm were constructed using a Singer model 4423 sewing machine, of white organdy (JoAnn Fabrics and Crafts, Rohnert Park, CA), white polyester thread, and cinched with black 4 mm diameter parachute cord. These nets were placed over the entire plant and funnel assembly in April of 2020 and checked twice weekly.
Larvae were collected by cutting off ends of symptomatic branches of various hostplants and dissecting them using a scalpel under a Leica MZ75 stereomicroscope. Larvae were teased from their tunnels with a pin, and frozen before shipment to CDFA labs, or alternatively kept in ethanol 80%.
Pupae were recovered from the duff within the adult enclosures (above) and later from beneath heavily infested plants in the landscape. Cocoons were found about 5 cm beneath the surface of the duff, usually sandwiched between fragments of two dead leaves to which they were lightly attached.
We further added data obtained from observation platforms iNaturalist, BugGuide, and Barcode of Life Data Systems.
Genitalia were prepared according to standard procedures—those by DRD using Canada balsam as embedding medium, those by EvN usually including DNA extraction—and using Euparal as embedding medium; see earlier papers (
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 pseuduncus; 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 carinae. Total corpus bursa length was measured from where the ductus bursae widens into the corpus bursae to anterior edge of bursa. 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 stereomicroscope at a magnification of 20×. Antennal segment counts include scape and pedicel; they were counted on photographs or directly under the same stereo microscope. Larval measurements of potential 2nd, 3rd, and 4th instars, mounted on slides, were from San Rafael, California (Figs
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 and Zeiss AxioVision software to prepare a picture in full focus from a Z-stack of ca 10–40 individual photos. Genitalia were photographed with an MRc 5 camera on a manually operated Zeiss Axioskop H, without using extended focus. Photographs were edited with Adobe Photoshop (various versions), avoiding changes to the real object, but backgrounds were cleaned of excess debris and artifacts by using the healing brush and clone tools; tone and contrast are adjusted, and some sharpening was used. Larvae in fluid, as well as dry cocoons, pupal skin, and a parasitoid, were photographed with a Leica MZ 16 using LAS IV Z-stack, as above, and scanning electron microscopy of the larvae was done using a Vega 3 Tescan with normal vacuum; the samples were sputter-coated with gold palladium.
Our methodology has been described in other papers (
Hostplant names follow Catalogue of Life (
Etainia albibimaculella;
Holotype. United States • ♂; Arizona, Cochise Co., Huachuca Mts., Miller Canyon; 31.4248, −110.26; 5,200’ [1585 m]; 19.iii.1987; larva collected with Arbutus arizonica; R. S. Wielgus leg.; emerged 24.v.1987 [reared by D.L. Wagner], DLW Lot: 87C4.5; Genitalia slide EvN4950; USNM01850751.
Paratypes
(13♂, 6♀). United States – Arizona • 1♂; Cochise Co., Ash Canyon, Huachuca Mts.; 5100’ [1550 m]; 6.x.1979; P.M. Jump leg.; Genitalia slide USNM16408; USNM01850740 • 1♂; Yavapai Co., 20 km W. Prescott, Yavapai CG [Campground]; 9.vi.1997; oak-juniper-pine; H.W. van der Wolf leg.; Genitalia slide EvN5492;
Canada – Ontario • 1♀; Ottawa, 40 km W, Almonte; 7.ix.1992; Kauri Mikkola leg.; alvar, ad lucem; Genitalia slide EvN4138;
United States – California • 9 larvae in ethanol; Marin Co., 400 Deer Valley Rd., San Rafael, Smith Ranch Homes; 15.iii.2017; S.J. Seybold, S. Swain leg.; ex collected stems and leaves, Marina strawberry tree, Arbutus × ‘Marina’ (Arbutus unedo × A. andrachne);
possibly of E. thoraceleuca. United States – Washington • vacated mines; Washington, Chelan Co., Wenatchee National Forest, Entiat summit Road; 12.vii.2010; E.J. van Nieukerken leg.; EvN2010017; low Pinus ponderosa forest on ridge, leafmines on Arctostaphylos uva-ursi;
Canada – Ontario • 1♂, 1♀; Lambton Co., Port Franks; 21.viii.2021, 25.ix.2020; K. H. Stead leg.; BIOUG62319-H05, BIOUG74608-E04 (BOLD).
United States – Arizona • 1 adult; Cochise Co., Sierra Vista Southeast. Miller Canyon Upper Parking; 17.v.2022; Jim Eckert; https://www.inaturalist.org/observations/142023215. – California • 1 adult; San Diego Co., San Marcos; 31.vii.2018; Greg Smith leg.; https://bugguide.net/node/view/1568125 • 1 adult; Santa Clara Co., Silicon Valley, Stanford Academic Reserve; 5.vi.2021; Jen and Hilary Bayer leg.; Malaise trap; BIOUG92695-A02 (BOLD) • 1 adult; Tulare Co., Ash Mountain; 06.vii.2018; Graham Montgomery leg.; https://bugguide.net/node/view/1569217.
United States – California • Colusa Co., various localities; mines on Arctostaphylos manzanita; 27.ii.2020, 4–5.ii.2021, 27, 28.iii.2021; K. Schneider leg.; https://www.inaturalist.org/observations/72384123, https://www.inaturalist.org/observations/72335843, https://www.inaturalist.org/observations/72447513, https://www.inaturalist.org/observations/39306497, https://www.inaturalist.org/observations/69086879, https://www.inaturalist.org/observations/69119629 • Contra Costa Co., Mount Diablo State Park; leafmines on Arctostaphylos manzanita subsp. laevigata; 8.ii.2020; Ken-Ichi Ueda leg.; https://www.inaturalist.org/observations/38489869 • Los Angeles Co., Claremont, California Botanic Garden; 2 leafmines on Arctostaphylos insularis; Steven Kurniawidjaja leg.; https://www.inaturalist.org/observations/150883693 • Los Angeles Co., La Cañada Flintridge, Descanco Gardens; 2 leafmines on Arbutus; Steven Kurniawidjaja leg.; https://www.inaturalist.org/observations/155422286 • Marin Co., Santa Venetia, leafmine on unidentified host; 28.i.2020; Krissa Klein leg.; https://www.inaturalist.org/observations/38138633 • Modoc Co., FR-73, 0.1 road mi W Householder Reservoir entrance road; leafmines on Arctostaphylos manzanita; 17.v.2021; K. Schneider leg.; https://www.inaturalist.org/observations/79232102, https://www.inaturalist.org/observations/79232103 • San Diego Co., 31.iii.2019; leafmines on Arctostaphylos rainbowensis; James Bailey leg.; https://www.inaturalist.org/observations/21914712 • San Diego Co., Cleveland National Forest; 11.xi.2021; leafmines on Arctostaphylos; Jorge Ayón leg.; https://www.inaturalist.org/observations/100888480.
Etainia thoraceleuca is easily recognized by the combination of a white thorax and the silver markings: a fascia and costal plus dorsal spot. Some Stigmella species have a similar pattern, but can be recognized by the distinct collar, comprising lamellar scales. Most similar are some species of Acalyptris, including the eastern A. thoracealbella (Chambers, 1873). This species has the pattern not so silvery, the antennae are paler, and the wings are narrower; moreover, the distribution does not seem to overlap much, but genitalia should be checked when in doubt. The male genitalia are characteristic of the genus Etainia by the valval apodemes, absent uncus, and structure of the phallus; it differs from E. ochrefasciella and E. sericopeza by the different shapes of the valva and gnathos, and the latter are very wide in E. sericopeza and very narrow in E. ochrefasciella. The female genitalia differ especially by the different structure of tergite 8.
Male (Figs
Female (Figs
Male genitalia
(Figs
Female genitalia
(Figs
Egg. In the few examples seen on leaf underside, the usual domed egg scale of Nepticulidae. When the mine develops, the egg is more or less in the center of the leaf spot.
Larva (Figs
Larval whole body of Etainia thoraceleuca 18 first instar: a whole larva posterior (L) to anterior (R), dorsal view b close up head (ventral view) c close up posterior (dorsal view) 19 second instar (dorsal and ventral) 20 third instar (dorsal and ventral) 21 fourth instar (ventral-lateral).
Larval head and posterior end of Etainia thoraceleuca 22, 23 head capsule of instar 3? in slide, dorsal (22) and ventral (23) view,
Etainia thoraceleuca, larva, scanning electron microscopy [scale bars = µm] 29 early instar head ventro-lateral 30 early instar head ventral 31 early instar labium with spinneret, labial palps and maxillae with palps, ventral 32 mid instar dorsal spinneret and labial palps 33 mid instar dorsal spinneret 34 early instar spiracle A4 35 mid instar A8-A10 lateral 36 mid instar lateral A10 37 mid instar A8–A10 posterior lateral 38 early instar rows of spines in anal opening A10 39 early instar ventral A10 40 early instar lateral ventral A10. Scale bars: 100 µm (30, 35–37); 50 µm (29, 31); 20 µm (32, 34, 38–40); 10 µm (33).
Leafmine damage caused by Etainia thoraceleuca 41 Marin Co., CA: S. Swain, leafmine on Marina strawberry tree, Arbutus × ‘Marina’ 42 CA: Sonoma Co., S. Swain, leafmine on manzanita, Arctostaphylos spec. 43 CA: San Diego Co., S.J. Seybold, MA Siefker, coll., leafmine on Marina strawberry tree, Arbutus × ‘Marina’ 44 CA: Marin Co., S.J. Seybold, coll., mines on stems and leaves from manzanita, Arctostaphylos spec.
Active larvae of Etainia thoraceleuca boring in woody stems of Marina strawberry tree, Arbutus × ‘Marina’ from CA: Marin Co. unless otherwise mentioned 45–46 CA: Sonoma Co., S. Swain 47–50 open stem with larval head, dorsal view 51 larva in stem with anal rods visible 52 larva, removed from stem, attacked by a mirid nymph 53 Chalcidoid parasitoid, most likely Eulophidae: Entedoninae and cocoon of Etainia thoraceleuca with exit hole of parasitoid.
Pupa (skin) (Figs
Cocoon (Figs
Hostplants. Ericaceae: Arbutus arizonica (A. Gray) Sarg. (Arizona madrone), Arbutus menziesii Pursh (Pacific madrone), Arbutus × andrachnoides Link ‘Marina’, (Marina strawberry tree, possibly Arbutus unedo L. × A. andrachne L.), Arctostaphylos canescens Eastw. (
Life cycle. Eggs are apparently laid singly on the underside of leaves in late summer to early fall, where they remain quiescent for several weeks. In late fall, the larvae hatch and begin burrowing into leaf tissue. On the oviposition site there develops a red to black stained leaf spot; from there the larvae make a thin, linear mine running along the lateral and midveins of the hostplants’ leaves, often very straight or sometimes with a few loops; the frass line is central and almost completely fills the gallery; the mined area soon turns red to black. Larvae continue burrowing through the petiole and into subtending twigs where they mine phloem tissues. After feeding in the twig cambium for several months, larvae bore their way out of the twigs and drop into the leaf litter beneath the plant. The exit holes are little slits in the twig epidermis, resembling those of other nepticulids. On California’s north coast, this occurs from April to May. Larvae pupate in the duff, tying dead leaves and perhaps other organic material together with bright-saffron to orange silken cocoons. Pupation is complete by June with most adult moths emerging early to mid-May in 2019 and 2020. Moths were found between 26 April and 14 October, which may indicate two annual generations, or a rather irregular emergence of adults. Adults are usually found at light.
(Figs
As larvae from many leaves migrate into subtending twigs to feed, their numbers and associated damage become concentrated, damaging the cambium to such an extent that the distal portions of the twig are frequently killed. These branches wilt and die rapidly, leaving the wilted end of the twig to droop, shrivel, and then harden into a shepherd’s crook. Even when twigs are not killed, the bark splits and callus tissue will form on the twigs, disfiguring and sometimes distorting it. In severe cases, young Arbutus ‘Marina’ trees have been killed, and older trees rather severely disfigured, with less than 50% live canopy remaining. Damage to native manzanita and madrone does not appear to be as severe.
As might be expected for a moth in its native range, parasitoid wasp pupae have been found inside the mines on occasion. One Chalcidoidea parasitoid (most likely Eulophidae, Entedoninae, C. Eiseman pers. comm.) emerged in summer 2023 from cocoons from Sonoma (near Napa Co.) found by SVS on 11 May 2023; it made a circular exit hole on a broad cocoon surface (Fig.
(Figs
(Fig.
The identical barcodes of adults and larvae undoubtedly show that the described larvae and damage belong to the same species as the adults.
The specimens from Canada differ in having a completely orange head and in their female genitalia; in both specimens the signa are almost equal length, 360 μm. In a Californian female specimen one of the three rows of setae on T8 seems to be missing. The genitalia of the male Canadian specimen could not yet be examined. For now, we consider the Canadian specimens as belonging to the same species, but further study and material is required to evaluate the possibility of hidden diversity.
The specific name, thoraceleuca, a noun in apposition, is derived from the Greek noun thorax (breastplate) and adjective leukos (white), referring to the characteristic white thorax.
In a maximum-likelihood analysis of Nepticulidae based on a maximum of eight genes (to be published elsewhere), E. thoraceleuca groups with E. albibimaculella and the eastern Palearctic E. capesella (Puplesis, 1985) as sistergroup to all other Holarctic representatives of Etainia, which are probably all associated with Acer (Sapindaceae). The grouping of E. albibimaculella and E. capesella was also observed earlier (
The sister-group relationship between E. thoraceleuca and E. albibimaculella may suggest a scenario where the common ancestor invaded North America from Asia, where it continued on the same hostplant, Arctostaphylos uva-ursi and from there invaded the mountains in the West and expanded its host range to include the abundant other Ericaceae hostplants already present.
The three Canadian records, far away from most records from the western USA, suggest that the species may have a continuous distribution with the northern Arctostaphylos uva-ursi, which has a very wide distribution throughout Canada and the northern and western United States. It is remarkable, however, that this relatively large and conspicuous nepticulid has not been recorded anywhere else in Canada, and also not in the extensive Canadian Malaise trapping programs (
The genera Arbutus and Arctostaphylos are closely related and grouped in the subfamily Arbutoideae (
As Etainia thoraceleuca is indigenous in California, its occurrence on cultivated plants was to be expected and by itself not of much concern. In some cases, however, the damage made by the insect can become a nuisance, but the use of the neonicotinoid imidacloprid in many nurseries (personal communications to SVS) has probably prevented this from becoming problematic. This, however, is in no way a plea to use these pesticides against this insect, as the damage caused by neonicotinoids to insects, especially bees, is too well known (
This paper is dedicated to the late Steven Seybold (formerly Department of Entomology and Nematology, University of California - Davis and USDA Forest Service, Davis, CA), who had a productive career as a Forest Entomologist and initiated parts of this study. Specimens were provided by him via Dave Wagner (University of Connecticut), Drew Zwart (Bartlett Tree), and Megan Siefker (formerly at UC Davis), who provided assistance for Dr Seybold and after his untimely death, brought MEE his larval specimens and leaf damage vouchers. David Bettman and Chris C. Ginter (California Academy of Science) located an old Keifer specimen and added fruitful insights. K. Schneider, Camiel Doorenweerd, and Frank Stokvis (Naturalis) are acknowledged for DNA analysis and Mollyanne Meyn (Mira Exterior Design) for her help in obtaining access to privately held infested sites, and her thoughtful observations. Providing loans were the late Jerry Powell (Essig Museum, University of California - Berkeley), Lauri Kaila (Helsinki), and Angela Telfer and Jeremy DeWaard (
The authors have declared that no competing interests exist.
No ethical statement was reported.
No funding was reported.
Morphological study adults: EvN, DRD, Morphological study immatures: ME, EvN, Fieldwork, study of biology: SVS, Data compilation, writing: EvN, ME, SVS.
Erik J. van Nieukerken https://orcid.org/0000-0002-5721-1840
Marc E. Epstein https://orcid.org/0000-0001-8659-5815
The data that support the findings of this study are available in the main text and in datasets https://www.gbif.org/dataset/42e8fdc3-bcff-45ba-b318-605173ab1f04 and https://doi.org/10.5883/DS-ETAARB.