Research Article |
Corresponding author: Peter Michalik ( michalik@uni-greifswald.de ) Academic editor: Borislav Guéorguiev
© 2017 Joachim Schmidt, Peter Michalik.
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:
Schmidt J, Michalik P (2017) The ground beetle genus Bembidion Latreille in Baltic amber: Review of preserved specimens and first 3D reconstruction of endophallic structures using X-ray microscopy (Coleoptera, Carabidae, Bembidiini). ZooKeys 662: 101-126. https://doi.org/10.3897/zookeys.662.12124
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The ground beetle genus Bembidion is a highly diverse group of small predators with more than 1.200 described extant species. In contrast, only two representatives of Bembidion are known from the amber fossil record and their position within this mega-diverse genus is dubious. Here, we address the taxonomic position of these two extinct Bembidion species (B. succini Giebel, 1856 and B. christelae Ortuño & Arillo, 2010). Based on the insufficient description and the missing type specimen, B. succini, nomen dubium, cannot be assigned to the genus Bembidion and/or to the tribe Bembidiini with certainty. The subgenus Archaeophilochthus Ortuño & Arillo, 2010 was erected for the second extinct species, B. christelae, based on external characters. However, this species seems indistinguishable to members of the earlier described subgenus Philochthemphanes Netolitzky, 1943 which comprises about extant 10 species distributed in East and Southeast Asia. Furthermore, we describe two new species, B. bukejsi sp. n. and B. alekseevi sp. n., from the Eocene Baltic amber using X-ray microscopy. Based on external and genital morphology including endophallic structures, we erected the monotypic subgenus Eodontiumsubgen. n. for B. bukejsi sp. n., which is probably related to the subgenera Andrewesa Netolitzky, 1931, the Hydrium complex, or the Odontium series sensu
Ground beetles, Archaeophilochthus , Eodontium new subgenus, new species, 3D reconstruction, Eocene, Christian Gottfried Giebel collection
Ground beetle fossils of the mega-diverse genus Bembidion preserved in Baltic amber are frequently mentioned in catalogues of amber inclusions (
The specimen was studied and imaged using light microscopy and micro-CT. The methods and technology used were described in detail in previous works by
Measurements of the fossil specimen were taken as follows: body size was quantified by the standardized body length, i.e., the sum of: (1) the distance from the apex of the right mandible in closed position to the cervical collar, (2) the median length of the pronotum, (3) the distance from the base of the scutellum along the suture to the apex of the left elytron. The width of the head, of the pronotum, and of the elytra was measured at their widest points. The width of the pronotal apex was measured between the tips of the apical angles, the width of the pronotal base was measured between the tips of the laterobasal angles.
Bembidium succiniGiebel, 1856: 64.
B. succini was described from Baltic amber and it is the first fossil species described in this genus to species level. Although it was mentioned in catalogues of Baltic amber fossils (
The original description of B. succini, however, does not provide information to which genus of ground beetles this species actually belongs.
„Das einzige Bernsteinexemplar der Leipziger Universitätssammlung ist kaum eine Linie lang und nähert sich zunächst den lebenden B. brunnicorne, B. perplexum, ist jedoch noch schmäler und gestreckter als diese, das Halsschild mit weniger convexen Seiten, die Flügeldecken mit feinen Punktstreifen, das ganze Tierchen hellgrün. Leider umgibt eine Blase das Thierchen so, daß ich weder die Beine noch die Palpen deutlich erkennen kann und nur aus den übrigen Formverhältnissen auf die Gattung Bembidium schließe“ (
Based on the few character states presented in this description it cannot be excluded that the name B. succini is given to a tiny (body length not even 2.3 mm) representative of the subtribe Tachyina or even to an Eocene species of a non-Bembidiini lineage.
Unfortunately, the taxonomic position of B. succini has remained ambiguous since all Baltic amber fossils of the Christian Gottfried Giebel collection are missing today. About 150 years ago, the fossil collection of Giebel was completely moved from the palaeontological collections of the Leipzig University to the University of Halle where it is now part of the geoscientific collections of the Institute of Geosciences and Geography. In 1973 parts of this collection were loaned to the Bulgarian Academy of Sciences for further study and were probably returned to Halle in 1998, however, details of the transfer of the material as well as its current location are unknown (
Bembidion (Archaeophilochthus) christelaeOrtuño & Arillo, 2010: 190.
A monotypic subgenus Archaeophilochthus Ortuño & Arillo, 2010 was established for the fossil B. christelae. In the subgeneric diagnosis, the authors mentioned the following six features to be important for assigning the taxon: (i) elytral discal setae each are inserted in the third interval separated from the third stria; (ii) the groove of the rounded humeral margin ends “close to the 4th or 5th striae” (Ortuño and Arillo, 2010: 191, subgeneric diagnosis) and “at the base of 6th interstriae” (p. 190, species diagnosis), respectively; (iii) humeral setae of the elytral umbilicate series grouped and +/- equidistant; (iv) pronotal basolateral fovea poorly delimited; (v) pronotal laterobasal angles with carina well developed; vi) pronotal laterobasal angles formed oblique.
Because the first five of these features are similarly developed in Philochthus Stephens, 1828,
Two extant Bembidion subgenera have been identified to be closely related to Philochthus (
Male in Baltic amber; size of amber piece approximately 8.9 × 4.7 × 2.5 mm (Fig.
The amber piece and its Bembidion fossil are in a comparatively very good conservation state. Most parts of the piece are clear, and the beetle body is well visible using light microscopy (Figs
One stellate hair and numerous dirt particles.
Body length: 3.5 mm.
Colour: The whole body surface appears blackish, very shiny, with metallic lustre; variation in colouration of the different parts of the beetle body is not recognizable.
Microsculpture: Surface of head including labrum with deeply engraved isodiametric sculpticells, pronotum with less deeply engraved slightly transverse meshes, elytral intervals with very finely engraved transverse meshes which are much smaller than on head and pronotum and which are not visible below magnification of ×100.
Head: Moderately large and transverse; length 0.75 mm, width 0.80 mm. Mandibles moderately slender. Labrum with apical margin slightly concave, dorsally with three pairs of setae near apical margin. Clypeus with one pair of setae in normal position. Shape and setation of maxillary palpi as typical for Bembidion, with apical segment subulate, approx. 2/5 of length of penultimate segment; penultimate segment markedly broadened towards apex. Antennae rather short, with pedicellus approx. 1.5 times longer than broad, and with two antennomeres extending beyond the pronotal base. Mentum and submentum distinct, mentum with medio-apical tooth simple, shortly rounded at tip, and with one pair of setae; pits absent. Eyes large, hemispherical, protruded; tempora very small, approx. 1/20 of eyes diameter, not visible in dorsal view. Disk moderately convex, smooth apart from the prominent microsculpture. Frontal furrows very shallow, very short, absent on disk. Supraorbital furrows flat, without punctures; two supraorbital setae present and in normal position for Bembidion.
Prothorax: Pronotum moderately large, length 0.76 mm, width 1.04 mm, transverse (width/length = 1.37), 1.3 times broader than head, subcordate, broadest slightly before middle, with sides faintly concave in posterior third. Laterobasal angles large, almost rectangular, not protruded laterally. Basal margin 1.1 times broader than apical margin. Disk moderately convex, smooth. Anterior margin finely convex in middle, lateroapical angles distinctly protruded, rounded. Posterior margin not beaded, slightly convex in middle, slightly sinusoidal towards laterobasal angles, latter very faintly shifted anteriad with respect to posterior margin of pronotum. Median longitudinal impression deep in middle, deepest before posterior transverse impression, but absent near pronotal apex and base; anterior transverse impression very shallow, smooth; posterior transverse impression moderately deep, smooth; laterobasal foveae large and rounded, moderately deep, smooth. Lateral gutter narrow throughout, smooth. Laterobasal carina long and straight, approx. 1/3 of length of pronotum. Both lateral and laterobasal setae present, with the lateral seta located slightly before middle of pronotum. Proepisternum glabrous, smooth.
Pterothorax: Elytra moderately convex on disc, in dorsal view narrow ovate, length 2.05 mm, width 1.37 mm, length/width = 1.50, widest near anterior third, distinctly wider than pronotum (width of elytra/width of pronotum = 1.32). Surface and lateral border glabrous and smooth apart from the primary elytral setation. Shoulders moderately broad with humeral margin angulate: The lateral bead forms an almost right angle with the abbreviated basal bead; the latter extends to the tip of the 4th elytral stria. Crista clavicularis absent. Sides with preapical sinuation indistinct; subapical plica present. Parascutellar stria moderately long, parascutellar seta present. All striae complete, deeply impressed, impunctate, with intervals convex; apical stria (= common prolongation of the 5th, 6th, and 7th striae) deeply impressed from level of the apical cross of 5th and 6th stria towards apex; recurrent stria lacking. Ninth interval moderately broadened from level of humeral umbilicate series towards apex. Each elytron with two discal setae in third interval, with relevant pores located close to, but separated from, third stria. Preapical seta located in the deepened apical portion of the seventh stria; the fine apical seta located at apical margin. Umbilicate series consist of eight setae: four humeral setae, with distance between first and second as well as second and third setae slightly larger than that between third and fourth setae; the fourth seta is located distinctly basad of the level of the anterior discal seta; both the subapical setae are markedly advanced and located at the beginning of the apical elytral third; two apical setae of the umbilicate series situated anterior of the junction of the eighth stria and lateral gutter. Metepisternum long, glabrous and smooth, with outer margin 1.6 times longer than anterior margin. Metasternal process without borders, moderately convex in middle. Hindwings fully developed.
Abdomen: Abdominal sternites V–VII each with one (male) pair of setae near apical margin; surfaces smooth, without hairs or micropunctures.
Legs: Relatively short, unmodified, femora moderately robust, protibiae straight and moderately dilated towards apex. First protarsomere markedly dilated, second protarsomere moderately dilated with apicolateral projection on inner margin.
Male genitalia (Figs
Bembidion bukejsi sp. n., holotype, volume rendering of selected body parts 9 caudal aspect of body 10 tarsomeres and distal portion of tibia of right proleg. 11 frontal section of body (ventral aspect) showing position of the abdominal segment IX which surrounds the aedeagus 12 abdominal segment IX and aedeagal median lobe, left lateral aspect 13 sagittal section of aedeagal median lobe, left lateral aspect. Abbreviations: antc = antecosta; bow-l = left wall of basal orfice; bsc-fd = folding structures originating from the endophallic brush sclerite; cfd = central folding system of endophallus; csc = central sclerite of endophallus (left lobe); dpl = dorsal plate of endophallus; mla = aedeagal median lobe apex; mlb = aedeagal median lobe base; mlw-d = dorsal wall of median lobe; mlw-v = ventral wall of median lobe; mtg IX = mediotergite IX; omp = ostial microtrichial patch; pm-l = left paramere (basal portion).
Bembidion bukejsi sp. n., holotype, visualization of endophallic structures using micro-CT. 14 volume rendering of the aedeagal median lobe with sclerotized endophallic structures highlighted in colors 15–16 parts of transverse sections through the abdomen with aedeagus (for position of slices see Fig.
The species epithet is a dedication to the collector Andris Bukejs, which kindly allowed us to investigate this unique specimen.
The angulate humeral margin together with the position of the elytral discal setae separated from third stria and the shape of the endophallic structures provide important evidence for probable relationships of the fossil species. An angulate humeral margin is also developed in species of the Bembidion sensu lato lineages Andrewesa Netolitzky, 1931, Hoquedela Müller-Motzfeld, 1988, Peryphophila Netolitzky, 1939, Phyla Motschulsky, 1844, Plataphodes Ganglbauer, 1891, as well as in the Hydrium and Odontium complexes sensu
Based on a comprehensive phylogenetic analysis of Bembidion and related ground beetles,
Aedeagal median lobes and endophallic structures of recent Bembidiina (18–25) and the fossil Bembidion bukejsi sp. n. (26), left lateral view. 18 Hoquedela k. kirschenhoferi Müller-Motzfeld, 1988 19Bembidion (Phyla) tethys Netolitzky, 1926 20B. (Plataphus) f. fellmanni Mannerheim, 1823 21B. (Melomalus) altaicum Gebler, 1833 22B. (Peryphophila) eurydice Andrewes, 1926 23B. (Andrewesa) patris Schmidt, 2010 24B. (Bracteon) lapponicum Zetterstedt, 1828 25B. (Odontium) striatum Fabricius, 1792 26B. (Eodontium) bukejsi subgen. n., sp. n. (Fig.
The external shape of the aedeagal median lobe and sclerotization patterns of the endophallic structures present in B. bukejsi sp. n. resemble those of species of Andrewesa (Fig.
Molecular data suggest that Andrewesa is the sister group of the Hydrium complex, while the Odontium complex is the sister group of the Hydriomicrus complex; both the latter taxa together form the Odontium series (
We could not find additional derived characters justifying a further assignment of the fossil species B. bukejsi sp. n. with one of these three lineages of the OPO clade. Similarities with representatives of extant species groups are considered to be symplesiomorphies, e.g., the shape of the pronotum and the development of the elytral striation. In B. bukejsi sp. n., the pronotal basolateral foveae are large and rounded as in Andrewesa. In many species of the Hydrium complex and in all species of the Odontium series, the basolateral foveae are linear impressed, and the area between foveae and laterobasal carina is markedly wide and convex. The latter represent apomorphic states. The elytral striae are deeply impressed throughout in B. bukejsi sp. n., and likewise in Hydriomicrus Casey, 1918, Hirmoplataphus Lindroth, 1963, and Pseudoperyphus of the Odontium series. In all the remaining lineages of the Odontium series as well as in Andrewesa and the Hydrium complex, the external elytral striae are more or less distinctly more shallowly impressed before the apex. Latter is considered an apomorphic character state.
Due to the impunctate elytral stria B. bukejsi sp. n. differs strikingly from all species of Andrewesa, the Hydrium complex and the Odontium series. However, impunctate or indistinctly punctate elytral striae are also present in other lineages of the clade, e.g., Melomalus, the Ocydromus series, and the Plataphus complex. This character shows also continuous variation in other Bembidiina clades and is therefore not informative with regard to its phylogenetic implications.
Due to the peculiar combination of the character states observed in B. bukejsi sp. n., we conclude that this fossil species represents an extinct lineage of the OPO clade, probably related to either Andrewesa plus the Hydrium complex or the Odontium series, or to both of these sub-clades. Given the present state of knowledge, the assignment to one of the known subgeneric taxa is impossible and therefore we decided to describe a new subgenus for this fossil representative of Bembidion (see below).
The above mentioned OPO clade represents one of the most species rich clades of Bembidion sensu lato (
Bembidion bukejsi sp. n.
The new subgenus name is an abbreviated combination of “Eocene” and “Odontium” and thus combines the period of the Earth history when the type species of the new subgenus lived, with the name of a probably related subgeneric taxon of Bembidion.
An extinct lineage of the OPO clade based on the combination of the seven male genital characters mentioned in the description of B. bukejsi sp. n. above. From most lineages of this highly diverse clade, Eodontium subgen. n. is distinguished by the presence of an angulate humeral margin and by the elytral discal setae, which are separated from the third stria. From all species of the subgenus Andrewesa and of the Hydrium and Odontium complexes which have these character states similarly or identically developed, Eodontium subgen. n. is easily distinguished by the impunctate elytral stria. The Eocene lineage differs additionally from Andrewesa by the thoroughly deeply impressed elytral striae and by the lack of elytral transverse depressions, and from the Hydrium and Odontium complexes by the large, roundish, deeply impressed laterobasal foveae of the pronotum, which is also distinctly less bulged on disc. Moreover, most species of the latter complexes differ markedly by the shape of pronotum, which has a base distinctly broader than apical margin and basolateral area between foveae and side margin convex.
An angulate humeral margin is also developed in High Asian subgenus Peryphophila and some species of the Holarctic Plataphus complex. However, in these lineages of the OPO clade the elytral discal setae are situated in the third stria. In addition, the endophallic central sclerite complex is much smaller compared to Eodontium subgen. n.
Female in Baltic amber; size of amber piece approximately 14 × 12 × 4 mm (irregularly cut, Fig.
The amber piece is permeated by broad light-reflecting flow lines particularly at level of the Bembidion inclusion. The anterior portion of the ventral side of the beetle body is covered by milky coating. Thus, mouth parts, ventral side of prothorax, and some portions of the dorsal surface of the fossil cannot by investigated by light microscopy (Figs
Syninclusions. Few dirt particles, numerous air bubbles.
Description. Body length: 3.9 mm.
Colour: Head and pronotum blackish brown with marked metallic lustre. Elytra middle brown with yellowish side margin (eighth and part of the seventh intervals), a small yellowish pre-apical spot between sixth and eighth interval at the beginning of the apical elytral third, and additionally with small yellowish spots in the third (4 spots) and fifth intervals (3 spots) as shown in Fig.
Microsculpture: Surfaces of head including labrum and pronotum with deeply engraved isodiametric sculpticells. Elytral intervals with very finely engraved, small and irregularly formed meshes which are not clearly visible below magnification of ×100.
Head: Moderately large and transverse; length 0.84 mm, width 0.91 mm. Mandibles moderately stout. Labrum with apical margin slightly concave, dorsally with three pairs of setae near apical margin. Clypeus with one pair of setae in normal position. Apical segment of maxillary palpus subulate, approx. 2/5 of length of penultimate segment; penultimate segment rather long and slender, moderately dilated anteriorly. Antennae moderately slender, with pedicellus almost two times longer than broad, and with four antennomeres extending beyond the pronotal base. Mentum and submentum distinct (shape and setation of medio-apical tooth could not be recovered); pits absent. Eyes large, hemispherical protruded; tempora very small, approx. 1/16 of eyes diameter. Disk slightly convex, smooth apart from the prominent microsculpture. Frontal furrows very shallow, very short, absent on disk. Supraorbital furrows very shallow, without punctures; two supraorbital setae present and in usual position for Bembidion. The pore of the anterior supraorbital seta is semicirculary surrounded by a prominent ridge on its internal side (Fig.
Prothorax: Pronotum rather small, length 0.77 mm, width 1.02 mm, transverse (width/length = 1.32), 1.1 times broader than head, subcordate, broadest in middle, with sides distinctly concave in posterior third. Laterobasal angles large, slightly obtuse, not protruded laterally. Basal margin 1.05 times broader than apical margin. Disk moderately convex, smooth apart from the prominent microsculpture. Anterior margin slightly convex in middle, lateroapical angles small and rounded, slightly protruded. Posterior margin not beaded, distinctly convex in middle and concave near laterobasal angles. Median longitudinal impression moderately deep in middle, absent near pronotal apex and base; anterior and posterior transverse impressions very shallow, smooth; laterobasal foveae large and rounded, moderately deep, smooth. Lateral gutter narrow and flat, faintly widened in middle, smooth. Laterobasal carina long and straight, approx. 1/3 of length of pronotum. Both lateral and laterobasal setae present, with the lateral seta located slightly before middle of pronotum. Surface structures on ventral side of the prothorax could not be imaged.
Pterothorax: Elytra in lateral view moderately convex, slightly flattened on disc, in dorsal very slender ovate, length 2.34 mm, width 1.52 mm, length/width = 1.54, widest slightly behind the middle, distinctly wider than pronotum (width of elytra/width of pronotum = 1.49). Surface and lateral border glabrous and smooth apart from the primary elytral setation. Shoulders moderately broad, humeral margin rounded, sides with preapical sinuation indistinct. Presence or absence of crista clavicularis as well as subapical plica could not be imaged. Parascutellar stria long, parascutellar seta present. All striae complete, slightly impressed but markedly punctate, intervals flat or slightly convex; apical stria deeply impressed from the apical cross of 5th and 6th stria towards apex; recurrent stria lacking. Ninth interval very narrow in front, slightly broadened from beginning of apical third towards apex (the left elytron of the specimen is artificially flattened in anterior third and therefore, the external intervals appearing distinctly broader caudally than on the right elytron, see Figs
Bembidion alekseevi sp. n., volume rendering of the head capsule of the holotype using different grayscale thresholds, dorsal aspect. The arrow in Fig.
Abdomen: Abdominal sternites V–VI with one, VII with two (female) pairs of setae near apical margin; surfaces smooth, without hairs or micropunctures.
Legs: Moderately short, unmodified, femora moderately robust, protibiae straight and moderately dilated towards apex.
Female genitalia: Could not be recovered using micro-CT.
The new species is dedicated to Vitalii I. Alekseev, Kaliningrad, for his important contributions to the systematics and biogeography of Cenozoic Coleoptera.
This fossil Bembidion is considered to be a representative of the subgenus Eupetedromus Netolitzky, 1911 based on combination of the following characters: (i) micro-meshes on surface of head and pronotum deeply engraved and thus contrasting with the elytra which appearing polished when viewed by magnification below x80; (ii) penultimate segment of maxillary palpus rather slender; (iii) anterior supraorbital pore on internal side semicirculary surrounded by a prominent ridge; (iv) supraorbital furrows very shallow; (v) pronotal median longitudinal impression not deepened near base; (vi) pronotal posterior transverse impressions very shallow; (vii) elytral discal setiferous pores distinctly separated from third stria; (viii) distance between third and fourth setae of the umbilical humeral series much larger than between first and second and between second and third setae. Similar patterns of elytral chaetotaxy are also observed in other species groups of Bembidion, e.g., Emphanes Motschulsky, 1850, Notaphemphanes Netolitzky, 1920, Notaphocampa Netolitzky, 1914, Notaphus Dejean, 1821, Omotaphus Netolitzky, 1914, Talanes Motschulsky, 1864, Trepanedoris Netolitzky, 1918, Trepanes Motschulsky, 1864, and the Diplocampa complex sensu
The subgenus Eupetedromus contains ten species which are distributed in the temperate and boreal zones of the Holarctic region (
At least three species of Bembidion are currently known to occur in the Baltic amber forests, which can be assigned to very different lineages of the genus (phylogeny based on Maddison, 2012). Thus, the mega-diverse genus Bembidion was likely already rich in species during the Eocene. Furthermore, this suggests that the discovery of additional Bembidion species fossilized in Paleogene deposits is very likely.
The assignment of the fossil species to certain Bembidion lineages results in preliminary conclusions regarding the habitat preferences of the fossil taxa and the ecological conditions in the Amber forests. Since extant species of the subgenus Philochthemphanes possess a semi-arboreal life style and are adapted to very humid forests with high density of epiphytes in the shrub and tree layers, it seems very likely that similar conditions were present in the Baltic Amber forests and that B. christelae was a likewise semi-arboreal beetle, which could have been easily trapped by the freshly leaked resin while climbing on the tree bark.
All extant Philochthemphanes species are adapted to temperate climates. Although the distribution of this subgenus in East Asia reaches far into tropical latitudes, occurrences of Philochthemphanes in these regions are restricted to high mountains and consequently, to the corresponding colder temperature conditions of the respective local climate. In addition, species of the proposed sister group, the subgenus Philochthus, as well as B. (Lindrochthus) wickhami, which is closely related to the Philochthus-Philochthemphanes clade based on molecular data (
The general assumption that the Baltic Amber forest occurred in the paratropical to subtropical zone of the Eocene (
We thank Andris Bukejs (Daugavpils) and Vitalii I. Alekseev (Kaliningrad) for providing the pieces of amber with the Bembidion inclusions for study. Particular thanks are due to Alexander Anichtchenko (Daugavpils) for pointing us to the existence of new fossil ground beetle species preserved in the A. Bukejs collection. We thank Frank Bach (Geological-Paleontological Collection of the University of Leipzig) and Norbert Hauschke and Meinolf Hellmund (Institute of Geosciences and Geography, University of Halle) for the information regarding history and probable location of the Giebel amber collection. We are very grateful to David Maddison (Corvallis, USA) and Luca Toledano (Verona, Italy) for their important and helpful comments. The study was supported by the German Research Council (DFG SCHM 3005/2-1, INST 292/119-1 FUGG and INST 292/120-1 FUGG).