Revisiting the morphology and systematic placement of the enigmatic Cretaceous ommatid beetle Bukhkalius lindae (Coleoptera: Archostemata: Ommatidae)

The systematic position of Bukhkalius lindae (Jarzembowski et al. 2017) from mid-Cretaceous Burmese amber is revised based on a re-examination of the type specimen. Our observations confirm that B. lindae lacks unique apomorphies of Tetraphalerus Waterhouse, in which it was originally placed, including complete antennal grooves and mushroom-shaped micro-tubercles. It is well justified to place it into a separate genus, i.e., Bukhkalius Kirejtshuk & Jarzembowski, 2020. The incomplete but distinct antennal grooves and the Tetraphalerus-like mouthparts of B. lindae suggest that it has a close affinity to Tetraphalerus. Therefore, B. lindae may represent a missing link bridging the morphological gap between extant ommatid subfamilies Tetraphalerinae and Ommatinae.


INTRODUCTION
Extant Ommatidae is a small archostematan family, which can be divided into two subfamilies, Ommatinae sensu stricto and Tetraphalerinae (Bouchard et al., 2011). Extant Tetraphalerinae comprises a single genus, Tetraphalerus Waterhouse, and two species, T. bruchi Heller and T. wagneri Waterhouse. Both occur in the southern half of South America (Hörnschemeyer & Beutel, 2016). Seven apomorphies of Tetraphalerus have been identified by a morphology-based phylogenetic analysis, including head with antennal grooves below the eyes and mushroom-shaped micro-tubercles inserted with minute scales (Hörnschemeyer, 2009).
Since Ponomarenko (1964), numerous Mesozoic compression-impression fossils have been placed in the extant genus Tetraphalerus by various authors (summarized in Kirejtshuk, 2020). However, the most characteristic feature of Tetraphalerus, ventrolateral antennal grooves, was not detectable in any of these compression-impression fossils. Recently, Jarzembowski et al. (2017) reported a new species, T. lindae Jarzembowski et al, 2017, from mid-Cretaceous Burmese amber, and assigned it to Tetraphalerus. The specimen, although nicely preserved, was poorly photographed and illustrated in Jarzembowski et al. (2017), which hindered an accurate evaluation of its systematic position within Ommatidae. Kirejtshuk & Jarzembowski (in Kirejtshuk, 2020) later recognized that T. lindae is probably not a member of the genus Tetraphalerus, and therefore erected a new genus Bukhkalius Kirejtshuk & Jarzembowski to accommodate B. lindae (Jarzembowski et al., 2017). Unfortunately, the diagnosis of Bukhkalius was insufficiently proposed to justify such a taxonomic act. In this paper, we aim to clarify the external morphology of B. lindae based on new images under epifluorescence and confocal microscopy to evaluate its systematic position within the Ommatidae. Sciences, Nanjing, China, was re-examined. Additional Omma specimens in NIGP were also examined for comparison. The specimens were derived from amber mines near Noije Bum Village (26°20′N, 96°36′E), Hukawng Valley, Kachin State, northern Myanmar (Jarzembowski et al., 2017). The amber piece containing B. lindae was further ground with emery papers of different grit sizes and polished with polishing powder to improve the visibility of the beetle's ventral side.

MATERIAL AND METHODS
Photographs under incident light were taken with a Zeiss Discovery V20 stereo microscope. Widefield fluorescence images were captured with a Zeiss Axio Imager 2 light microscope combined with a fluorescence imaging system. Confocal images were obtained with a Zeiss LSM710 confocal laser scanning microscope. Images under incident light and widefield fluorescence were stacked in Helicon Focus 7.0.2 or Zerene Stacker 1.04. Confocal images were manually stacked in Adobe Photoshop CC. Images were further processed in Adobe Photoshop CC to enhance contrast. Revised diagnosis: Body elongate. Head moderately elongate; temples short; antennal grooves short, only reaching anterior margin of eyes; antennae short, subfiliform; separate mentum present. Pronotal disc without protuberances or ridges; propleura not reaching anterior prothoracic margin; procoxae contiguous. Elytra with indistinct longitudinal ridges (primary veins); lateral edge of elytra with double rows of teeth. Abdominal ventrites abutting.

Systematic
Bukhkalius differs from Tetraphalerus in head only moderately elongate, antennal grooves incomplete, and mushroom-shaped micro-tubercles absent. Bukhkalius differs from the remaining genera in Ommatidae in the combination of antennal grooves present (though incomplete), separate mentum present, and propleura not reaching anterior prothoracic margin.

Remarks:
The diagnosis provided in Kirejtshuk (2020) was insufficient, which cannot really differentiate Bukhkalius from Omma and Omma-like genera. For example, he claimed that "this new genus [Bukhkalius] differs from the genera with subglobous prothorax (Cionocoleus, Cionocups, Omma, Polyakius and Rhopalomma) in the clear 'neck' of the head". However, neck is clearly present in both extant (Escalona et al., 2020) and fossil ommatines. The neck in some fossil Omma (Figs. 4B, C) could be even narrower than that of Bukhkalius.
Abdomen with five coplanar ventrites, separated by wide grooves; first and fifth ventrites longer than others.

DISCUSSION
Bukhkalius lindae was originally placed in the extant genus Tetraphalerus by Jarzembowski et al. (2017). In fact, it has many characters different from extant Tetraphalerus based on our examination. The most important feature defining the extant Tetraphalerus is the presence of distinct antennal grooves on the ventrolateral side of the head, which extend up to the posterior margin (Beutel et al., 2008). Although Jarzembowski et al. Li, Y-D. et al.: Redescription of Bukhkalius lindae Pap. Avulsos Zool., 2021; v.61: e20216128 2/6 (2017) mentioned that the lateral notch between protuberance P1 and P2 may indicate a presence of antennal grooves for B. lindae, our observation clearly shows that it lacks complete antennal grooves (Fig. 3A). Extant species of Tetraphalerus have mushroom-shaped micro-tubercles, each inserted with a short and stout seta (Hörnschemeyer, 2009). It is clear that B. lindae does not possess this special form of micro-tubercles. Indeed, to our knowledge, such a peculiar structure is not known in any other extant or fossil archostematan beetles. Extant species of Tetraphalerus have a strongly elongated head, i.e., more than 1.3× longer than wide (Hörnschemeyer, 2009), whereas the head of B. lindae (excluding neck) is approximately as long as wide (Fig. 3A). Besides, we were unable to detect the well-developed protuberance above eye (P2) in B. lindae as illustrated in fig. 2 in Jarzembowski et al. (2017). Based on these morphological differences, we suggest that it is plausible to place B. lindae into a separate genus.
Interestingly, B. lindae displays some similarities with the extant Tetraphalerus. In extant Ommatinae (Omma Newman and Beutelius Escalona et al., 2020), if the propleuron is not fused with the prosternum, the notopleural suture is complete and never joined by the pleurosternal suture, i.e., propleuron reaches anterior prothoracic margin (Escalona et al., 2020; incorrectly coded in Lawrence et al., 2011). In contrast, the propleuron of the extant Tetraphalerus does not reach the anterior prothoracic margin, even though it is very close (Friedrich et al., 2009;R.G. Beutel, pers. comm.; incorrectly coded in Beutel et al., 2008). Similarly, the propleuron of B. lindae also seems not to reach the anterior prothoracic margin (Fig. 3B). The in Beutel et al., 2008) are very alike, though the maxillary palps of B. lindae is longer. In extant Ommatidae there is a sensorial cavity on the apical maxillary palpomere. The apical maxillary palpomere is expanded in Omma and Beutelius, so the cavity tends to be relatively small compared to the palpomere (figs. 4-7 in Lawrence, 1999). In contrast, the apical maxillary palpomere is slender in Tetraphalerus, so the cavity is relatively large ( fig. 3D in Beutel et al., 2008). The shape and relative size of the cavity on the apical maxillary palpomere of B. lindae match well with that of Tetraphalerus (Fig. 3A). In most archostematans a separate mentum is absent (although Escalona et al., 2020 described a mentum in Omma and Beutelius, the mentum actually corresponds to the prementum as defined by Beutel et al., 2008 andHörnschemeyer, 2009), whereas the mentum of Tetraphalerus is recog-nizable as a transverse sclerite between submentum and prementum (Beutel et al., 2008;incorrectly coded in Hörnschemeyer, 2009). A distinct transverse mentum is also present in B. lindae (Fig. 3A). Besides, in B. lindae there is a pair of possibly short antennal grooves, extending merely to the anterior edge of the compound eyes (Fig. 3A). Here we tentatively suggest that this structure may represent an early evolutionary stage of the well-developed antennal grooves in extant Tetraphalerus. Given the above discussions, we suggest that the enigmatic Bukhkalius is probably an early lineage closely related to the South America endemic Tetraphalerus and should be included in Tetraphalerinae. Numerous Mesozoic "Tetraphalerus" species have been reported from Russia (e.g., Ponomarenko, 1966), Mongolia (e.g., Ponomarenko, 1997), Kazakhstan (e.g., Ponomarenko, 1964), Kyrgyzstan (Ponomarenko, 1969), Spain (e.g., Soriano & Delclòs, 2006), and China (e.g., Tan et al., 2007Tan et al., , 2012. Ponomarenko (1969) even proposed two series, each including one of the only two extant Tetraphalerus species (T. bruchi and T. wagneri), to accommodate the Mesozoic "Tetraphalerus" species. His practice of placing Mesozoic "Tetraphalerus" into series was followed by other researchers (e.g., Soriano & Delclòs, 2006;Tan et al., 2007). In the cladistic analysis of Tan et al. (2012), the fossil "Tetraphalerus" species (including Tetraphalerites Crowson) form a monophyletic group together with extant species of Tetraphalerus. This Tetraphalerini clade was united by a single non-homoplasious change, i.e., the presence of ventrolateral antennal grooves on head. However, the character coding of their analysis was problematic. In Tan et al. (2012), all three Mesozoic "Tetraphalerus" fossils were coded as having antennal grooves. No antennal grooves, however, were mentioned in the original descriptions of "T. " brevicapits Ponomarenko & Martínez-Delclòs or "T. " glabratus Ponomarenko (Ponomarenko, 1997;Ponomarenko & Martínez-Delclòs, 2000), and we failed to detect the antennal grooves in the original figures either. Contradictorily, Tan et al. (2012) even clearly stated that no antennal grooves were visible in "T. decorosus" (name actually unavailable due to failure to comply with the requirements of ICZN, see Dubois et al., 2013) in the description part of their own paper. To our knowledge, the most critical character of Tetraphalerus, ventrolateral antennal grooves, was not discernible in any Mesozoic specimens belonging to "Tetraphalerus". Although Tan & Ren (2009) claimed that the presence of antennal grooves is clearly evident in "T. " curtinervis Tan et al., 2012, we cannot identify this structure based on the photos provided in the paper. Other vital diagnostic features, including the relatively  large mushroom-shaped micro-tubercles and a separate mentum, were also not reported in these Mesozoic "Tetraphalerus". Therefore, we agree with Kirejtshuk (2020) that probably none of the Mesozoic species of "Tetraphalerus" should be placed in Tetraphalerus. The divergence between Ommatidae and Micromalthidae has been dated to Early Cretaceous, approximately 130 Ma (McKenna et al., 2019). It is reasonable to expect the divergence between two extant species of Tetraphalerus to happen much later than that. As such, it makes no sense to place the Early Cretaceous, or even Jurassic fossils into the T. bruchi and T. wagneri series.

ACKNOWLEDGMENTS
We are grateful to Prof. Rolf G. Beutel for helpful discussion, Mr. Yan Fang for technical help in confocal imaging, and Mr. Dao-Jun Yuan for help in inspecting the holotype of Bukhkalius lindae deposited at NIGP.