Article | Open | Published:

Specialized adaptations for springtail predation in Mesozoic beetles

Scientific Reportsvolume 7, Article number: 98 (2017) | Download Citation

Abstract

Insects exhibit a variety of morphological specializations specific to particular behaviors, and these permit the reconstruction of palaeobiological traits. Despite the critical importance of predator-prey strategies in insect evolution, the appearance of particular aspects of predation are often difficult to determine from the fossil record of hexapods. Here we report the discovery of highly specialized, mid-Cretaceous ant-like stone beetles (Staphylinidae: Scydmaeninae) displaying morphological modifications unknown among living scydmaenids and associated with predation on springtails (Collembola), a widespread and abundant group of significantly greater geological age. Cascomastigus monstrabilis gen. et sp. nov. exhibits an extremely large body size, elongate clubbed maxillary palpi, toothed mandibles, and more importantly, slender and highly modified antennae that functioned as an antennal setal trap. Such an antennal modification is analogous to that of the modern ground beetle genus Loricera (Carabidae: Loricerinae), a group possessing a specialized antennal setal trap exclusively for the capture of springtails. The presence of an identical antennal setal trap in C. monstrabilis demonstrates a unique and dramatic form of obligate predation among the late Mesozoic insects.

Introduction

Predator-prey interactions are a critical component of ecological and evolutionary associations, shaping the success (or lack thereof) of major lineages. Specific associations are often difficult to discern in the fossil record, despite the extensive record of predatory and parasitic taxa in most deposits. This dearth of direct observational evidence for particular predator-prey associations gives the false impression that most extinct species of insect predators were perhaps generalists owing to the absence of data suggesting otherwise. Specialized predator systems are difficult to document in the absence of either extraordinary preservation or unique morphological traits directly correlated with particular biologies.

Springtails (Hexapoda: Collembola), usually only a few millimeters long, are one of the most widespread and abundant of terrestrial arthropods, and is the most diverse group of Entognatha, the sister group to insects. The clade has a global distribution, occurring on every continent, including Antarctica, and species are often found as ‘aerial plankton’1. One of the most remarkable and characteristic structures of springtails is their specialized jumping organ (furcula), which has evolved through the basal fusion of a pair of appendages on the fourth abdominal segment and acts like a spring when released from an associated, ventral locking mechanism1, 2. Although some have secondarily lost their jumping organs, most springtails are capable of jumping for a long distance, and this leaping has apparently evolved for both dispersion as well as an effective means of predator avoidance. The earliest known Collembola, Rhyniella praecursor, from the Early Devonian Rhynie chert (Scotland, approximately 400 million years ago [mya]), is strikingly modern in appearance relative to the surviving family Isotomidae, to which the species likely belongs3, 4. These fossils demonstrate that springtails established their specialized mode of locomotion over 400 million years ago3, 5. Given their ubiquity and abundance, a wide range of animals are general predators of Collembola1, while specialized predators of springtails are limited6. Among the known specialized predators are some beetles, wasps, and ants, and in each various body parts or organs are modified for hunting springtails in different manners6. Fossil evidence of such specialized predation on springtails, however, has been lacking. The recent discovery of ant-like stone beetles, belonging to the extant staphylinid tribe Mastigini, in mid-Cretaceous amber from Myanmar provides a unique example of a specific and early predatory-prey association, and reveals a group specialized for predation on the abundant resource represented by springtails.

Results

Systematic Palaeontology

Order Coleoptera Linnaeus, 1758

Family Staphylinidae Latreille, 1802

Subfamily Scydmaeninae Leach, 1815

Supertribe Mastigitae Fleming, 1821

Tribe Mastigini Fleming, 1821

Cascomastigus monstrabilis Yin & Cai, gen. nov

LSID, urn:lsid:zoobank.org:act:08FE9CB6-4F93-4F68-B397-F2B6D392AF36

Type species

Cascomastigus monstrabilis Yin & Cai, sp. nov. (here designated)

Diagnosis

Cascomastigus are separated from other genera of the Mastigini by the following combination of characters: body size exceptionally large (usually over 6.5 mm); maxillary palpus extremely elongate, with enlarged apical palpomere (palpomere IV) strongly bent basally; and elytron distinctly striate.

Cascomastigus monstrabilis Yin & Cai, sp. nov

LSID, urn:lsid:zoobank.org:act:7D363AB7-A803-4B30-A375-7AF3B46E88CF

Type material

Holotype, SNUC-Paleo-0005, male, housed in the Insect Collection of the Shanghai Normal University, Shanghai, China. Paratype, NIGP165026, female, housed in the Nanjing Institute of Geology and Palaeontology, CAS, Nanjing, China. Both specimens are derived from the earliest Canomanian amber (approximately 99 mya) from Hukawng Valley, Kachin State, northern Myanmar.

Diagnosis

As for the genus (see above), with the following minor additions: antenna slightly shorter than body; scape 1.30 (female)–1.62 (male) times as long as head, and 0.96 (female)–1.13 (male) times as long as pronotum; antennomere IV 1.3 (male)–1.8 (female) times as long as III.

Description

Refer to online Supplemental Information for a complete description and etymology.

Discussion

The three specimens presented here belong to two different species of a new genus — Cascomastigus monstrabilis (both sexes known; Fig. 1), and an unnamed species Cascomastigus (female). Cascomastigus are unambiguously referred to the extant ant-like stone beetle supertribe Mastigitae, a small group of Scydmaeninae (Staphylinidae), based on multiple putative synapomorphies: antennomere I (scape) elongate, much longer than antennomere II (pedicel) (Fig. 2a); antenna distinctly geniculate between scape and pedicel (Fig. 2f); maxillary palpus longer than head, with palpomere IV slightly longer than palpomere III and strongly asymmetrical (Fig. 2f); and compound eyes located in the anterior part of the head7, 8. Moreover, Cascomastigus are placed in the extant tribe Mastigini based on the presence of two longitudinal rows of robust spines on the basal two antennomeres (Fig. 2a), antennomere II broader than the flagellomeres (Fig. 2a), and the apical maxillary palpomere broader than palpomere III (Fig. 2d). The discovery of three definitive mastigine fossils extends the earliest records of the tribe by about 54 million years, the next oldest being those species in mid-Eocene Baltic amber (approximately 45 mya)9.

Figure 1
Figure 1

Habitus of Cascomastigus monstrabilis (a,b: male, SNUC-Paleo-0005; c,d: female, NIGP165026). (a) Dorsolateral view. (b,c) Lateral view. (d) Dorsal view. Scale bars: 2 mm.

Figure 2
Figure 2

Morphological details of Cascomastigus monstrabilis (ae: male; f,g: female). (a) Left antenna. (b) Left antennomere I. (c) Left antennomere II, and an enlarged image of a single basal socket. (d) Left maxillary palpus. (e) Right mesotarsomeres. (f) Head in lateral view, showing antennomeres I–II and maxillary palpi. (g) Same, in dorsal view. Abbreviations: a1–11, antennomeres I–XI; e, compound eye; ma, mandible; mp, maxillary palpus; mp1–4, maxillary palpomeres I–IV; ps, postgenal setae; ts1–5, tarsomeres I–V. Scale bars: 1 mm in A and E; 500 μm in others.

With a body length about 6.9 mm, these Cretaceous Cascomastigus are markedly larger than most extant Scydmaeninae (usually less than 2 mm long), and are indicative of Mastigitae, a group including the largest known Scydmaeninae (approximately 10 mm long). Like the modern mastigine genus Stenomastigus, the legs and antennae of Cascomastigus are extremely slender and elongate (Fig. 2a,b). The long legs, including tarsi (Fig. 2e), are probably suggestive of active and rapid locomotion. Like their modern counterparts, Cascomastigus likely moved quickly on substrates, likely the forest floor (soil or humus layer). The hind wings are not visible and the elytra are strongly constricted basally, tending to indicate that Cascomastigus were likely flightless, similar to many extant mastigines. Considering the extremely similar body form and greatly extended appendages to those of extant species, Cascomastigus were likely also diurnal predacious beetles, occurring in loose layers of leaf litter, and on the soil surface10. The elytra of Cascomastigus are distinctly striate, with each elytron bearing six longitudinal punctate striae (Supplementary Figs 1b and 2a,b). This feature is not known among extant Mastigini, but somewhat similar elytral punctures partly arranged in longitudinal rows can be found in the Eocene Baltostigus 9. Cascomastigus bear elongate maxillary palpi, with slightly enlarged and basally bent apical palpomeres (Fig. 2d). By contrast, the apical maxillary palpomeres of Baltostigus are strongly enlarged and axe-shaped9, a character more reminiscent of that of extant members of Mastigini, suggesting that the fossils may form a group sister to the remainder of the tribe. This is supported by the putatively primitive form of the elytra, along with the slightly enlarged apical maxillary palpomere in both groups. The mandibles of Cascomastigus have a sharp preapical tooth and apex (Fig. 2f,g), suggesting a predatory lifestyle, as in modern mastigine beetles.

The most remarkable feature of Cascomastigus is the densely spiny antennal scape and pedicel (Fig. 2a–c, f,g; Supplementary Fig. 2c), and similarly dense, strong and long bristles are only found in Baltostigus (Supplementary Fig. 3a). The first antennomere (scape) is elongate and enlarged in all known Mastigitae, but it is armed with rows of bristles only in Mastigini. Compared to those of extant genera, the bristles on the scape and pedicel of Cascomastigus are much denser and larger (Fig. 2a–c). The scape of Cascomastigus, as long as the following four antennomeres combined, is armed with about 17 strong lateroventrally directed bristles arranged in two regular longitudinal rows (Fig. 2b). The long bristles on the scape gradually increase in length towards apex, with the apical bristles slightly shorter than the penultimate one (Fig. 2b). Similar to the scape, the pedicel is broad and elongate, about 6.5 times as long as the third antennomere (Fig. 2c). The pedicel bears about 13 lateroventrally directed bristles, which gradually shorten apically (Fig. 2c). By contrast, the following nine antennomeres are not morphologically specialized and devoid of such long bristles (Fig. 2a). All bristles are gradually tapered, with the greatest diameters at their bases (Fig. 2b,c). The bristles on the scape range from 0.26 mm to 0.81 mm in length, with average length about 0.46 mm distributed mainly in the median part. The bristles on the pedicel range from 0.25 mm to 0.62 mm in length, with average length about 0.48 mm. The bristles on scape and pedicel are largely of symmetrical, as evidenced by their similar lengths and relatively constant spacing (Fig. 2a), and more importantly, by the fact that the antennal scape bears a ventral notch, so that the pedicel can bend ventrally (Fig. 2f). Another interesting feature is that the most apical bristle on the scape and the most basal bristle on pedicel are somewhat of central symmetry (Fig. 2a), enabling these two bristles to form a functional setal pair when the antennae are folded. All of the lateroventrally directed bristles stand at right angles relative to the antennal length, so that bristles on the inner margins cross each other when the basal two antennomeres are brought together (Fig. 2g). When the antennae are folded, the scape and pedicel together form a well closed “cage” (Fig. 2f), representing a form of specialization perfectly analogous to that of the modern ground beetle genus Loricera (Carabidae: Loricerinae)11, 12. The sockets of these bristles are robust, with their openings facing lateroventrally (Fig. 2c), making the bristles unable to bend upwards. This structure is perfectly analogous to the functional, ventrally positioned setae on the basal antennomeres of species of Loricera 12. This antennal setal trap is used for preying upon springtails in Loricera, a commonly encountered hexapod living on the same damp, shady soil as these beetles11, 12. The presence of an antennal setal trap that corresponds so perfectly in structure to that found among Loricera strongly suggests that the similar trap in Cascomastigus was likely used for similar purposes.

Collembola are of considerable antiquity and include some of the earliest fossils of all hexapods. As noted, the earliest springtail, R. praecursor from the earliest Devonian, can be putatively attributed to an extant family, demonstrating a remarkable conservatism in their general morphology3, 4. Given their small sizes and soft bodies, the fossil record of Collembola is rather sparse, with only one other occurrence from the Paleozoic13. However, by the Cretaceous and the prevalence of amber deposits, ideally suited for the preservation of such minute arthropods, there is a diverse and rich record of springtails (summarized by Sánchez-García and Engel)14, and in some localities and pieces they can be numerous15,16,17,18,19. Burmese amber harbors one of the most diverse faunas of Collembola, represented by 14 described species in 13 genera16. Most Cretaceous collembolans are remarkably similar to their extant relatives, emphasizing the antiquity and considerable morphological stasis of the group17. Collembola would have been an abundant resource for predators in the Burmese amber environment, assuming they could be caught. Cascomastigus, with the aid of their specialized antennal setal trap, probably preyed on springtails occurring in the same habitat. Moreover, modern springtails often form large aggregations, and such aggregations are not uncommon in Burmese amber (Supplementary Fig. 3b). Like their extant counterparts, Cascomastigus probably moved quickly on the soil surface, enabling frequent encounters with prey such as springtails10. The antennae of Cascomastigus were likely largely stretched forward during movement, similar to the posture preserved in the holotype of C. monstrabilis (Fig. 1a,b). When stimulated by a potential prey, C. monstrabilis likely snapped the antennae together (Fig. 1c,d), bent the pedicel, and pushed its head against the ground. The prey would be caught in the trap formed by the strong bristles and then seized by the mouthparts.

Although all extant mastigines lack huge and strong bristles on the scape and the pedicel, the Eocene Baltostigus do possess bristles similar to those of Cascomastigus (Supplementary Fig. 3a)9. Thus, a more parsimonious explanation for the evolution of antennal bristles would be that the inconspicuous retention of small bristles on the scape and the pedicel of all extant taxa is secondarily derived, with the condition in the fossils plesiomorphic. On the other hand, it is also possible the presence of thickened bristles in Cascomastigus and Baltostigus are a derived condition, and became extinct in subsequent evolutionary events. Like the Cretaceous Cascomastigus, the Eocene Baltostigus were likely capable of trapping prey using the antennal bristles. There was apparently a shift of feeding habits (prey choice) during the evolutionary history of Mastigini: early mastigines, including Cascomastigus and Baltostigus, probably fed on fast-moving animals, presumably early springtails; whereas all extant mastigines (Mastigus, Palaeostigus, and Stenomastigus) feed on slow-moving organisms such as caterpillars or scavenge dead arthropods. Consequently, during the long evolutionary process, the scape and pedicel of extant mastigines might have reverted to a more typical function, no longer serving in prey capture, and becoming reduced in size.

The extant tribe Mastigini display a disjunctive distribution (Fig. 3)10. Two genera, Mastigus and Stenomastigus, occur only in South Africa, whereas Palaeostigus are known from southern Europe and South Africa9. It is apparent that the extant genera of Mastigini represent only a fraction of the group's true diversity9, and the lineage perhaps experienced significant extinction over the last 100 million years. Along with Baltostigus from Poland and Lithuania (Baltic amber), our discovery of Cascomastigus from the earliest Late Cretaceous amber of northern Myanmar further highlights the once broader distribution of Mastigini (Fig. 3). It also suggests that Mastigini appeared comparatively early, no later than the mid-Cretaceous (approximately 99 mya). Interestingly, Burmese amber harbors a relative rich fauna of scydmaenines20, although none of those had such antennal modifications. The mastigine forms with a functional antennal setal trap appear to have persisted for at least 54 million years.

Figure 3
Figure 3

Spatiotemporal distribution of extant and amber-embedded Mastigini. Recent distribution of Mastigini is represented in red. Mastigini-yielding fossil localities are indicated in blue for Baltostigus (Baltic amber), and in pink for Cascomastigus (Burmese amber). The temporal distribution of fossil and extant Mastigini is indicated by arrows of the corresponding colors. (The original map source was obtained from http://www.simplemappr.net, an on-line tool for creating maps that can be freely used for publications and presentations).

Despite their abundance, obligate predators of springtails are of low diversity6. Among the known specialized collembolan predators, various ground-dwelling beetles adopt different preying strategies for capturing springtails (Fig. 4). Such beetles belong to the Staphylinidae (rove beetles: some Stenus) and Carabidae (ground beetles: Leistus, Loricera, and Notiophilus). Specifically, Stenus catch elusive prey using a specialized adhesive prey-capture apparatus, which is modified from the labium21, 22. Leistus possess a hunting apparatus formed of strong setae in a circular arrangement on the ventral head surface23. Adults of Loricera have the aforementioned antennal setal trap11, 12; while larvae have elongate and strong maxillae with a long and tacky galea for hunting springtails24. Notiophilus hunt their prey based on visual acuity25. In addition, unusual adaptions for collembolan predation are also found in some wasps and dacetine ants6. Therefore, it is apparent that different morphological modifications for catching Collembola have originated independently for multiple times among insects. There are records of Stenus and Loricera in Baltic amber26,27,28,29, but only Stenus archetypus preserves an exposed adhesive prey-capture apparatus29. Two Stenus are recorded from the Cretaceous, but these are insufficiently preserved and specialized mouthparts, if they occurred, are unknown26, 27. A specialized larva of Loricera electrica with strong maxillae and bulb-shaped galeae has been reported from Baltic amber28, and an undescribed adult of Loricera with a typical antennal setal trap has also been recovered from the same deposits (Supplementary Fig. 3c,d). Thus, all previously known specialist predators of springtails are confined to the middle Eocene. The discovery of Cascomastigus from the mid-Cretaceous represents the earliest known predators specialized for capturing Collembola, pushing back the age of such predation by at least 54 million years.

Figure 4
Figure 4

Time-dated chronogram of specialist predators of Collembola in various insect groups. Their respective predatory strategies are provided at the right.

Methods

All amber pieces were cut by a handheld engraving tool with a diamond blade, then ground with emery papers of different grain sizes, and finally polished with polishing powder. Photographs were taken using a Canon EOS 5D Mark III digital camera, equipped with a Canon MP-E 65 mm macro lens (F2.8, 1–5X), and with an attached Canon MT-24EX twin flash. Focus stacking software (Zerene Stacker, Version 1.04) was used to increase depth of field. All images were modified and arranged in Adobe Photoshop CS5 Extended.

Additional information

Accession codes: This work is registered in ZooBank under LSID (Life Science Identifier) urn:lsid:zoobank.org:pub:27AFD033-D6E8-425F-A27B-DC06CDB64E34. The ZooBank LSID for the new genus and species is as follows: Cascomastigus LSID, urn:lsid:zoobank.org:act:08FE9CB6-4F93-4F68-B397-F2B6D392AF36; Cascomastigus monstrabilis LSID, urn:lsid:zoobank.org:act:7D363AB7-A803-4B30-A375-7AF3B46E88CF.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.

    Hopkin, S. P. Biology of the springtails (Insecta: Collembola) (Oxford: Oxford University Press) (1997).

  2. 2.

    Zhang, F., Sun, D. D., Yu, D. Y. & Wang, B. X. Molecular phylogeny supports S-chaetae as a key character better than jumping organs and body scales in classification of Entomobryoidea (Collembola). Sci. Rep. 5, 12471, doi:10.1038/srep12471 (2015).

  3. 3.

    Whalley, P. & Jarzembowski, E. A. A new assessment of Rhyniella, the earliest known insect, from the Devonian of Rhynie, Scotland. Nature 291, 317 (1981).

  4. 4.

    Greenslade, P. & Whalley, P. E. S. The systematic position of Rhyniella praecursor Hirst & Maulik (Collembola). The earliest known hexapod. In Second International Symposium on Apterygota (ed Dallai, R.) 319–323 (University of Siena, Siena, 1986).

  5. 5.

    Grimaldi, D. A. & Engel, M. S. Evolution of the Insects (Cambridge University Press, New York 2005).

  6. 6.

    Masuko, K. Studies on the predatory biology of Oriental dacetine ants (Hymenoptera: Formicidae) II. Novel prey specialization in Pyramica benten. J. Nat. Hist. 43, 825–841 (2009).

  7. 7.

    O’Keefe, S. T. Scydmaenidae Leach, 1815. In Handbook of Zoology, Coleoptera, Beetles, Vol. 1: Morphology and systematics (Archostemata, Adephaga, Myxophaga, Polyphaga partim) (eds Beutel, R. G. & Leschen, R. A. B) 280–288 (De Gruyter, New York, 2005).

  8. 8.

    Jałoszyński, P. Description of Euroleptochromus gen. n. (Coleoptera, Staphylinidae, Scydmaeninae) from Baltic amber, with discussion of biogeography and mouthpart evolution within Clidicini. Syst. Entomol. 37, 346–359 (2012).

  9. 9.

    Jałoszyński, P. A new Eocene genus of ant-like stone beetles sheds new light on the evolution of Mastigini. J. Paleontol. 89, 1056–1067 (2015).

  10. 10.

    Jałoszyński, P., Matsumura, Y. & Beutel, R. G. Evolution of a giant intromittent organ in Scydmaeninae (Coleoptera: Staphylinidae): Functional morphology of the male postabdomen in Mastigini. Arthropod. Struct. Dev. 44, 77–98 (2015).

  11. 11.

    Bauer, T. Predation by carabid beetle specialized for catching Collembola. Pedobiologia. 24, 169–179 (1982).

  12. 12.

    Hintzpeter, U. & Bauer, T. The antennal setal trap of the ground beetle Loricera pilicornis: a specialization for feeding on Collembola. J. Zool. Ser. A. 208, 615–630 (1986).

  13. 13.

    Riek, E. F. An entomobryid collembolan (Hexapoda: Collembola) from the Lower Permian of Southern Africa. Palaeontol. Afr. 19, 141–143 (1976).

  14. 14.

    Sánchez-García, A. & Engel, M. S. Springtails from the Early Cretaceous amber of Spain (Collembola: Entomobryomorpha), with an annotated checklist of fossil Collembola. Am. Mus. Novit. 3862, 1–47 (2016).

  15. 15.

    Christiansen, K. & Pike, E. Cretaceous Collembola (Arthropoda, Hexapoda) from the Upper Cretaceous of Canada. Cretaceous Res. 23, 165–188 (2002).

  16. 16.

    Christiansen, K. & Nascimbene, P. Collembola (Arthropoda, Hexapoda) from the mid Cretaceous of Myanmar (Burma). Cretaceous Res. 27, 318–363 (2006).

  17. 17.

    Sánchez-García, A. & Engel, M. S. Long-term stasis in a diverse fauna of Early Cretaceous springtails (Collembola: Symphypleona). J. Syst. Palaeontol., doi:10.1080/14772019.2016.1194575 (2016).

  18. 18.

    Azar, D., Gèze, R. & Acra, F. Lebanese amber. In Biodiversity of fossils in amber from the major world deposits (ed Penney, D.) 271–298 (Siri Scientific Press, Manchester, 2010).

  19. 19.

    Perrichot, V., Néraudeau, D. & Tafforeau, P. Charentese amber. In Biodiversity of fossils in amber from the major world deposits (ed Penney, D.) 192–207 (Siri Scientific Press, Manchester, 2010).

  20. 20.

    Chatzimanolis, S., Engel, M. S., Newton, A. F. & Grimaldi, D. A. New ant-like stone beetles in mid-Cretaceous amber from Myanmar (Coleoptera: Staphylinidae: Scydmaeninae). Cretaceous Res. 31, 77–84 (2010).

  21. 21.

    Bauer, T. & Pfeiffer, M. ‘Shooting’ springtails with a sticky rod: the flexible hunting behaviour of Stenus comma (Coleoptera; Staphylinidae) and the counter-strategies of its prey. Anim Behav. 41, 819–828 (1991).

  22. 22.

    Koerner, L., Gorb, S. N. & Betz, O. Functional morphology and adhesive performance of the stick-capture apparatus of the rove beetles Stenus spp. (Coleoptera, Staphylinidae). Zool. 115, 117–127 (2012).

  23. 23.

    Bauer, T. Beetles which use a setal trap to hunt springtails: the hunting strategy and apparatus of Leistus (Coleoptera, Carabidae). Pedobiologia. 28, 275–287 (1985).

  24. 24.

    Bauer, T. & Kredler, M. Adhesive mouthparts in a ground beetle larva (Coleoptera, Carabidae, Loricera pilicornis F.) and their function during predation. Zool. Anz. 221, 145–156 (1988).

  25. 25.

    Bauer, T. Prey capture and structure of the visual space of an insect that hunts by sight on the litter layer (Notiophilus biguttatus F., Carabidae, Coleoptera). Behav. Ecol. Sociobiol. 8, 91–97 (1981).

  26. 26.

    Schlüter, T. Zur Systematik und Palökologie harzkonservierter Arthropoda einer Taphozönose aus dem Cenomanium von NW-Frankreich. A: Geologie und Palaäontologie. Berliner Geowiss. Abh 9, 1–150 (1978).

  27. 27.

    Ryvkin, A. B. Novye Melovye Staphylynidae [sic!] (Insecta) s Dal’nego Vostoka. Paleontol. Zh. 1988, 103–106 (1988).

  28. 28.

    Klausnitzer, B. Käferlarven (Insecta: Coleoptera) in Baltischem Bernstein-Möglichkeiten und Grenzen der Bestimmung. Entomol. Abh. 61, 103–108 (2003).

  29. 29.

    Puthz, V. Stenus Latreille aus dem Baltischen Bernstein nebst Bemerkungen über andere fossile Stenus-Arten (Coleoptera, Staphylinidae). Entomol. Bl. Biol. Syst. Käfer. 106, 265–287 (2010).

Download references

Acknowledgements

Marius Veta (Palanga, Lithuania) provided the picture of Baltostigus used in Fig. S3A. Financial supports were provided by the National Natural Science Foundation of China (31501874, 41602009, 41688103, 91514302), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB18000000), the Ministry of Science and Technology (2016YFC0600406), the Natural Science Foundation of Jiangsu Province (BK20161091), and the Science and Technology Commission of Shanghai Municipality (15YF1408700).

Author information

Affiliations

  1. Department of Biology, College of Life and Environmental Sciences, Shanghai Normal University, Shanghai, 200234, P. R. China

    • Zi-Wei Yin
    •  & Li-Zhen Li
  2. Key Laboratory of Economic Stratigraphy and Palaeogeography, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, 210008, P. R. China

    • Chen-Yang Cai
  3. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, 210008, P. R. China

    • Di-Ying Huang

Authors

  1. Search for Zi-Wei Yin in:

  2. Search for Chen-Yang Cai in:

  3. Search for Di-Ying Huang in:

  4. Search for Li-Zhen Li in:

Contributions

Designed the project and wrote the manuscript: Z.-W.Y. and C.-Y.C. Participated in morphological studies and discussion: Z.-W.Y., C.-Y.C., H.-D.Y. and L.-Z.L.

Competing Interests

The authors declare that they have no competing interests.

Corresponding author

Correspondence to Chen-Yang Cai.

Electronic supplementary material

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/s41598-017-00187-8

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.