The elusive pygmy moth Bohemannia auriciliella (De Joannis, 1909): overview of its distribution, with new records for Germany and Bulgaria (Lepidoptera: Nepticulidae) Author Schulz, Tina Unter dem Sportplatz 15, D- 31552 Rodenberg, Germany t.s.r@gmx.de Author van Nieukerken, Erik J. Naturalis Biodiversity Center, PO Box 9517, NL- 2300 RA Leiden, The Netherlands nieukerken@naturalis.nl text Entomologische Zeitschrift: mit Insektenbörse 2020 2020-12-31 130 3 143 147 journal article http://doi.org/10.5281/zenodo.5093178 4a061fa8-3220-4701-b56e-7cf547917165 1860-1324 5093178 Introduction The pygmy moths ( Nepticulidae ) include some of the smallest moths in the world. In some species the winglength measures just over one millimetre ( GARCÍA-BARROS et al. 2017 ). Consistent with theirtiny size, little is known about the biology and distribution of many species, although the larval leafmines of the majorityof species are quite characteristic and more often found thanthe moths. Especiallywhenthe caterpillars do not make such mines, the distribution maps showstill manygaps as few people collect or photograph these tiny insects. Despite of being described over a hundred years ago, and being a relatively large nepticulid species (wingspan 6–7 mm), knowledge about the distribution of thespecies Bohemannia auriciliella ( DE JOANNIS, 1909 ) in Europeonly increased in thepast five decades. Including the new records presented here, 28 specimens of this species are now known from throughout Europe. Discovery and distribution It all starts in the year 1909 when Nepticula auriciliella was described by J. DE JOANNIS on one female specimen, collected in Vannes byhisbrother L. DE JOANNIS during the 17 preceding years (France, département Morbihan). Thespecies was more or less forgotten for 70 years, and KLIMESCH (1975) contributed to that by synonymizing it with Bohemanniaquadrimaculella (BOHEMAN, 1853) . Around the same time, another specimen was discovered in Kent ( Great Britain ). The well-known British Microlepidoptera specialist MAITLAND EMMET publishedthe find by E.S. BRADFORD in 1974 as a new species, Ectoedemia bradfordi EMMET, 1974 , also based on the advice of JOSEF KLIMESCH, who did not see the resemblance with JOANNIS’ type that he must have seen before. The secondspecimenof “ Ectoedemia bradfordi ” wasfoundamongst unidentified material in the collection of the Zoological Museum Amsterdam, caught already in 1931 in Hatert, near Nijmegen ( Netherlands ) ( VAN NIEUKERKEN 1982 ). Eventually, in 1986, the second author discovered the synonymy of the male Ectoedemia bradfordi EMMET, 1974 with the female Nepticula auriciliella DE JOANNIS, 1909 basedon externals, and recombined it with Bohemannia STAINTON, 1859 ( VAN NIEUKERKEN 1986a ). Soon thereafter he found an additional old specimen in the Copenhagen collection: a female moth from Southampton, accidentally reared in 1937 by W. FASSNIDGE (VAN NIEUKERKEN 1986b ). Step by step, more specimens were found. The Netherlands followed withtwomore records fromthe year 1988 (Meijnweg and Mariapeel). In the next decadeactive Britishand Dutchcollectors found more specimens: 1993 (Lover, South Wiltshire), Twello and Wageningen-Hoog (Gelderland 1996), and two moths from Gietelo (Gelderland) at the turn of the millennium. Additional records from Great Britain presumably document the activity of British microlepidopterists: moths were found in 2001 (Berkshire), 2003 (Hampshire), 2010 (Surrey), 2011 (Buckinghamshire), 2014 (Suffolk), 2015 (Southend-on-Sea) andreached the point of culmination in 2017 with three new records (Gloucestershire, Buckinghamshire and Worcestershire). Nevertheless, after 2000 thespecies also shows up in other European countries. In 2003 it appears in Czechia ( LIŠKA et al. 2005 ), and 2007 in Switzerland (SWISS-LEPTEAM 2010). The first record for Bulgaria is made in 2002 (Burgas; two specimens , leg. JARI JUNNILAINEN), here published for the first time, a second French specimen was collected in the Pyrenees (2010), and two new specimens were recently found in the Netherlands (2015, 2018), here recorded ( Table 1 , Fig. 5 ). Inthelight of thesedata, Germanywould perfectly fit in the distribution. Inthis paper the long awaited record is reported: on the 13th of June 2018 one specimenof Bohemannia auriciliella was collected on a sheet with 160 W mixed light, 2 x 18 W black light, 2x 20 Wsuperactinic light during a public mothing event in the Eilenriede, the city forest of Hannover. There, aroundthe “Waldstation” (which isa place to learn more about the forest‘s ecosystem) the biotope type can be classified as “Bodensaurer Buchenwald” (literally “beech forest on acidic soil”), with a tree ageof 65–130 years. Other treesoccurring there, besides European beech ( Fagus sylvatica , Fagaceae ), are Scots pine ( Pinus sylvestris , Pinaceae ), European spruce ( Picea abies , Pinaceae ), Europeanlarch ( Larix decidua , Pinaceae ), oaks ( Quercus sp. Fagaceae ), European black alder ( Alnus glutinosa , Betulaceae ), Silver birch ( Betula pendula , Betulaceae ) and Douglas fir ( Pseudotsuga menziesii , Pinaceae ). Since a few ponds have been laid out in close proximity to the “Waldstation”, the air humidity is relatively high. Figs 1, 2. Bohemanniaauriciliella ( DE JOANNIS, 1909 ) . 1. Female, Hannover, 13. June 2018, TLMF Lep 25991 (Photo: TINA SCHULZ ). 2. Male, Netherlands, Noord-Brabant, Riethoven, 26 June 2015, RMNH. INS.25160. SCale bar 1 mm (Photo: ERIK VAN NIEUKERKEN). Molecular analysis (Barcoding) Asampleof the Hanoverian specimen was sequenced by the Canadian Centre for DNA Barcoding (Guelph). The result was very surprising, and was confirmed by EvN whom TS sent a photoof themothper email. Three other specimens were barcoded in Leiden according to procedures as described before ( DOORENWEERD et al. 2016 , VAN NIEUKERKEN et al. 2012 ). In all now four specimens have been barcoded, and all show almost the same sequence, with Barcode Identification Number BOLD: ACG8823 , and a maximal distance of 0.16 %. The records can be seen on the BOLD Website: http://dx.doi.org/10.5883 /BOLD: ACG8823 . The Nearest Neighbour interestingly is the unrelated Gonionota amauroptera CLARK, 1971 , a Depressariidae from Argentina . Thebarcode distance to other known Bohemannia species is always larger than 15 % . Recognition Bohemanniaauriciliella ( Figs 1, 2 ) is relatively easy to recognise. It is one of the medium large Nepticulidae with a yellow head, wingspan 6–7 mm , collar rather small withlamellar scales (as in Stigmella species ) andscape (eyecap) withthe posteriorquarter grey (but thisis notthe case in one female ) and a relatively long antenna with 44–53 segments in male, 35– 38 in female. The forewing has a silver fascia beyond the middle, sometimes broken in two spots, and a brassy basal quarter. Bohemannia quadrimaculella (BOHEMAN, 1853) is larger, 7.0– 8.5 mm wingspan, has a uniform scape, antenna white tippedand forewingwithouta brassy base. Only some Stigmella species have a scape withadark edge, males of themuchsmaller S. betulicola (STAINTON, 1856) , S. alnetella (STAINTON, 1856) and the male of S. lemniscella (ZELLER, 1839) , but that has a black headand black androconialscales onthe hindwing. Seealso VAN NIEUKERKEN & JOHANSSON (1990) and LAŠTŮVKA & LAŠTŮVKA (1997) , also for genitalia illustrations. Themalegenitaliaare very characteristic ( Fig. 3 ), thefemale genitalialack the characteristic signa of most related species, theterminal segmentsof theholotype are illustrated in Fig. 4 . Discussion Considering the small size of this species and theonlyfewinterested partiesfor very small moths like Nepticulidae , it seemsnot so astonishing that Bohemannia auriciliella was discovered relatively late in Germany. Yet this has more reasons. There remains still someuncertaintyconcerning thehost plant and especiallytheimmature stages. What we know for sure is that adults occurbetweenlate Mayand August, with most records from June and early July. Thehost plant is thought tobe birch, mostly because the collection label of W. FASSNIDGE‘S specimen says it was reared from birch. EMMET (1987) suggested a scenario that FASSNIDGE reared themoth onlyaccidentally from branches collected to get Lampronia fuscatella (TENGSTRÖM, 1848), which lives in twig galls in birch. Unfortunately, there are no further notes by FASSNIDGE to enlighten this case. This was the exclusive record of a larva of B. auriciliella ; since then it has not been found again. Tab. 1. Synopsis of reCords of Bohemannia auriciliella ( DE JOANNIS, 1909 ) , listed more or less ChronologiCally, grouped by Country. GeographiC Coordinates Were in most instanCes derived from Google Earth.

Country, Location	Date	Number, Sex	Coordinates	Collector	Note/ References
F, Morbihan:Vannes	23.VI.(before 1909)	1♀	47.67N 2.73W	J.DE JOANNIS	Holotype, DE JOANNIS 1909
F, Pyrenées Or.: Caixas,La Serre	29.V.–19.VI.2010	1♀	42.582 N 2.6765E	B. WIKSTRÖM	RMNH.INS.25199,NeW reCord
NL, Gelderland:Hatert, near Nijmegen	21.VI.1931	1♂	51.804N 5.828E	LYCKLAMA à NIJEHOLT	RMNH.INS.20115, VAN NIEUKERKEN 1982 , 1986b
NL, Limburg: Mariapeel, near Helenaveen	17.VI.1988	1♀	51.403N 5.92E	J.H. KUCHLEIN	KUCHLEIN et al. 2000
NL, Limburg: MeijnWeg	9.VII.1988	1♂	51.173N 6.125E	G.R.LANGOHR	VAN NIEUKERKEN et al. 1993
NL, Gelderland:TWello	10.VII.1996	1♂	52.2426N 6.1084E	J.B.WOLSCHRIJN	KUCHLEIN et al. 2000
NL, Gelderland:Wageningen-Hoog	12.VII.1996	1♂	51.988N 5.6892E	J.H. KUCHLEIN	pers.Comm.J.KUCHLEIN
NL, Gelderland:Gietelo	11.VI.2000	1♀	52.183N 6.139E	J.B.WOLSCHRIJN	WOLSCHRIJN & KUCHLEIN 2001
NL, Gelderland:Gietelo	16.VI.2000	1♂	52.183N 6.139E	J.B.WOLSCHRIJN	RMNH.INS.23747, WOLSCHRIJN & KUCHLEIN 2001
NL, Noord-Brabant: Bergeijk, Riethoven	26.VI.2015	1♂	51.375N 5.422E	F.GROENEN	RMNH.INS.25160,NeW reCord
NL, Gelderland:Wageningen-Hoog	12.VI.2018	1♂	51.988N 5.6892E	J.H. KUCHLEIN	pers.Comm.J.KUCHLEIN
GB,Kent (VC15): Childs Forstal Wood, East Blean	7.VII.1973	1♂	51.337N 1.123E	E.S.BRADFORD	Holotype E.bradfordi, EMMET 1974 , VAN NIEUKERKEN 1986a
GB,Hampshire (VC11): Southampton	11.VII.1937	1♀	50.90N 1.40W	W.FASSNIDGE	VAN NIEUKERKEN 1986b
GB,South Wiltshire (VC8):Lover	24.VI.1993	1	50.978N 1.696W	M. F.W.CORLEY	CORLEY 1994
GB,Berkshire (VC22):Pine Wood	22.VI.2001	1	51.385N 0.793W	D.J.GIBBS	GIBBS 2002, LANGMAID & YOUNG 2002
GB,Hampshire (VC11): WiCkham Common	29.VI.2003	1	50.894N 1.16W	R.J.DICKSON	LANGMAID & YOUNG 2004
GB,Surrey (VC17): Knaphill	27.VI.2010	1♂	51.317N 0.615W	A.J.HALSTEAD	LANGMAID & YOUNG 2011
GB,BuCkinghamshire (VC24):Amersham, Hodgemoor Wood	2.VII.2011	1♂	51.632N 0.607W	P.HALL	HALL 2012
GB,Suffolk (VC25):Tangham Forest	21.VI.2014	1♂	52.075N 1.437E	A.WATSON	LANGMAID & YOUNG 2015
GB,Essex (VC18): Southend-on-Sea, Belfairs Woods	30.VI.2015	1♂	51.557N 0.635E	C.LEWIS	LEWIS 2015
GB,GlouCestershire (VC34): DymoCk Wood	19.VI.2017	1♂	51.953N 2.458W	G.H.J.MEREDITH	MEREDITH 2019
GB,BuCkinghamshire (VC24):BernWood Forest,Hell CoppiCe	21.VI.2017	1♂	51.788N 1.113E	P.HALL	HALL 2019
GB,WorCestershire (VC37):Shoulton	22.VIII.2017	1♂	52.226N 2.288W	P.CLEMENT	CLEMENT 2017
BG,Burgas,40 km SE:Ropotamo	5.VI.2002	2♂	42.27N 27.73E	J.JUNNILAINEN	RMNH.INS.23932,NeW reCord
CZ, Moravia: Lanžhot, Soutok	24.V.2003	1♀	48.618N 16.94E	J.LIšKA	LIšKA et al. 2005
CH,Canton of Geneva:Jussy	5.VI.2007	1♂	46.247N 6.288E	B.LANDRY & D. RUBINOFF	SWISSLEPTEAM 2010
DE,NiedersaChsen: Hannover	13.VI.2018	1♀	52.3898N 9.7887E	T.SCHULZ	TLMF Lep 25991,NeW reCord

Fig. 3. Male genitalia of Bohemannia auriciliella ( DE JOANNIS, 1909 ) . 3a. Ventral vieW. 3b. FoCussed more dorsally. Genitalia slide EvN5160, RMNH.INS.25160. SCale bars 100 μm (Photo: ERIK VAN NIEUKERKEN). Fig. 4. Female genitalia of Bohemannia auriciliella (DE JOANNIS, 1909), Holotype. Only the terminal segments are illustrated, as the bursa did not shoW any detail. 4a. Dorsal vieW. 4b. FoCussed more ventrally. Genitalia slide KL0720 (Photo: ERIK VAN NIEUKERKEN). If one considers that the main method to find pygmy moths is by searching their mining tracks, it seems clear thatthemine of B. auriciliella can not be easily recognised. So the larva‘s lifestyle is expected to be concealed; it is unlikely to be a leaf miner. Perhaps the larvalives inside abud orapetiole ( VAN NIEUKERKENet al. 1986b ), as it is known from a related species, Bohemannia quadrimaculella (BOHEMAN, 1853) , which most likely inhabits alder buds ( EMMET 1984 , VAN NIEUKERKEN 1986c ). Further, it may be interesting, that one moth was beaten from birch (VAN NIEUKERKEN et al. 1993), although all other specimens were swept from different bushes orlow vegetation, orcame to light, like the Hanoverian specimen did. At least one prominent silver birch is growing approximately ten metres apart fromthe sheetwhere it was collected. Nearby there are also black alders next to the ponds‘ edges. All Dutch records are also from relatively poorsandy soils with birch commonly present. However, itisdoubtful that birch occurs at the more Mediterranean localities in Bulgaria and the Pyrenees. Theelusive larvallife history is oneexplanation, but still B. auriciliella is muchless frequentlyfound than B. quadrimaculella , so that possiblyalso theadult is moreelusive and more difficult to find. Although B. auriciliella wasdescribed 111 years ago, its larva and lifecycle are still unknown. Furthermore, it is expected to be less scarce than it seems, as the known distributioncovers alarge part of Europe, and more andmore specimens are found, especially in countries with many active microlepidopterists. What we need, to prove this, isasuitable methodforfinding the larva. By now many Nepticulidae species can be recorded only by the larva ' s host plant and their way of mining. For B. auriciliella this approvedmethod hopefully is possible too – we are lacking only the knowledge to do so. This enigma shouldencourageus to finally disclosethe secret of its hidden biology. The recent finding and photographing of the similarlypoorlyknown larvalfeedingof Etainia species inwinter issomewhatpromising in this respect ( SOBCZYK et al. 2018 ).