New morphological and molecular data reveal an important underestimation of species diversity and indicate evolutionary patterns in European Lepidocyrtus (Collembola : Entomobryidae)
Eduardo Mateos A B F , Daniel Winkler C , Marta Riutort D B and Marta Álvarez-Presas D B EA Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Universidad de Barcelona, Avinguda Diagonal 643, E-08028 Barcelona, Spain.
B Institut de Recerca de la Biodiversitat (IRBio), Facultat de Biologia, Universitat de Barcelona, Avinguda Diagonal 643, E-08028 Barcelona, Spain.
C University of Sopron, Faculty of Forestry, Institute of Wildlife Management and Vertebrate Zoology, Bajcsy-Zsilinszky u. 4, HU-9400 Sopron, Hungary.
D Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Avinguda Diagonal 643, E-08028 Barcelona, Spain.
E School of Biological Sciences, University of Bristol, 24 Tyndall Avenue, Bristol, BS8 1TQ, UK.
F Corresponding author. Email: emateos@ub.edu
Invertebrate Systematics 35(5) 471-492 https://doi.org/10.1071/IS20016
Submitted: 30 March 2020 Accepted: 8 October 2020 Published: 28 June 2021
Abstract
The correct identification of morphological species is a key task for species richness estimation of any ecosystem. Although body colour is a widely used character identifying European Lepidocyrtus species, recent investigations using molecular data have revealed that species delineation using body colour can result in an underestimation of real species diversity because of the presence of cryptic species. Lepidocyrtus violaceus is a European species characterised by its dark violet body colour. Its wide distribution leads us to suspect that several cryptic species can be present within this morphospecies. Since traditional morphological characters have appeared insufficient for real diversity identification in Lepidocyrtus, new morphological characters were needed in order to describe the cryptic diversity detected by molecular data in this genus. Pseudopores are integumentary structures present in all Lepidocyrtus species, but the distribution of these structures has not been properly described in the genus, as well as in Entomobryioidea overall. In the present work we aimed to analyse whether L. violaceus is a monophyletic entity in Europe. Moreover, we aimed to determine if the position and number of pseudopores on the different parts of the body and appendages is a phylogenetically useful character in the identification of the species or superspecific entities. Fourteen populations of L. violaceus from five European countries, and another 25 Lepidocyrtus species from nine European countries have been studied. In total, 208 specimens have been analysed morphologically and half of them were studied molecularly using sequences of the genes COXII and EF-1α. Molecular data revealed that the widely distributed Lepidocyrtus violaceus morphospecies is a polyphyletic entity in Europe. Between 6 and 12 diferent cryptic species have been detected within this European morphospecies, and only the presence of pseudopores on the basal plate of the fourth abdominal segment has been found to be a promising diagnostic character between them. A common basal pattern of pseudopore distribution has been recognised in the European members of the genus, and also a diferential pattern within each European species group. As a general trend, an increase in the number of pseudopores has been detected from the most basal to the most derived species groups in the phylogeny of the genus in Europe.
Keywords: chaetotaxy, COXII, cryptic species, DNA, EF-1α, phylogeny, pseudopores, taxonomy.
References
Anslan, S., and Tedersoo, L. (2015). Performance of cytochrome c oxidase subunit I (COI), ribosomal DNA Large Subunit (LSU) and Internal Transcribed Spacer 2 (ITS2) in DNA barcoding of Collembola. European Journal of Soil Biology 69, 1–7.| Performance of cytochrome c oxidase subunit I (COI), ribosomal DNA Large Subunit (LSU) and Internal Transcribed Spacer 2 (ITS2) in DNA barcoding of Collembola.Crossref | GoogleScholarGoogle Scholar |
Barra, J. A. (1969). Collemboles du Gabon. Biologia Gabonica 5, 189–216.
Beck, J. (1873). Essay on the scales of the Collembola and Thysanura. In ‘Monograph of the Collembola and Thysanura’. (Ed. J. Lubbock.) pp. 249–254. (J. Ray Society: London, UK.)
Bellini, B. C., and Cipola, N. G. (2017). The Neotropical genera of Paronellinae (Collembola, Entomobryoidea, Paronellidae) with description of two new species and redescription of Campylothorax mitrai. Zootaxa 4300, 151–179.
| The Neotropical genera of Paronellinae (Collembola, Entomobryoidea, Paronellidae) with description of two new species and redescription of Campylothorax mitrai.Crossref | GoogleScholarGoogle Scholar |
Berg, M., and Heijerman, T. (2002). De springstaart Lepidocyrtus paradoxus nieuw voor de Nederlandse fauna (Hexapoda: Collembola). Nederlandse Faunistische Mededelingen 16, 69–75.
Christiansen, K. A., and Bellinger, P. F. (1980). ‘The Collembola of North America North of Rio Grande, a Taxonomic Analysis.’ (Grinell College: Grinnell, IO, USA.)
Cicconardi, F., Nardi, F., Emerson, B. C., Frati, F., and Fanculli, P. P. (2010). Deep phylogeographic divisions and long-term persistence of forest invertebrates (Hexapoda: Collembola) in the North-Western Mediterranean Basin. Molecular Ecology 19, 386–400.
| Deep phylogeographic divisions and long-term persistence of forest invertebrates (Hexapoda: Collembola) in the North-Western Mediterranean Basin.Crossref | GoogleScholarGoogle Scholar | 20015142PubMed |
Cicconardi, F., Fanciulli, P. P., and Emerson, B. C. (2013). Collembola, the biological species concept and the underestimation of global species richness. Molecular Ecology 22, 5382–5396.
| Collembola, the biological species concept and the underestimation of global species richness.Crossref | GoogleScholarGoogle Scholar | 24112308PubMed |
Cipola, N. G., and Bellini, B. C. (2016). A new cave species of Coecobrya Yosii (Collembola, Entomobryidae, Entomobryinae) from South Africa, with an identification key to the genus. Zootaxa 4200, 351–366.
| A new cave species of Coecobrya Yosii (Collembola, Entomobryidae, Entomobryinae) from South Africa, with an identification key to the genus.Crossref | GoogleScholarGoogle Scholar |
Cipola, N. G., de Morais, J. W., and Bellini, B. C. (2016a). A new genus of Entomobryinae (Collembola, Entomobryidae) from Brazilian Amazon with body scales and dental spines. Zootaxa 4105, 261–273.
| A new genus of Entomobryinae (Collembola, Entomobryidae) from Brazilian Amazon with body scales and dental spines.Crossref | GoogleScholarGoogle Scholar | 27394776PubMed |
Cipola, N. G., de Morais, J. W., and Bellini, B. C. (2016b). A new epigeous species of Troglobius (Collembola: Paronellidae: Cyphoderinae) from Brazil and notes on the chaetotaxy of the genus. The Florida Entomologist 99, 658–666.
| A new epigeous species of Troglobius (Collembola: Paronellidae: Cyphoderinae) from Brazil and notes on the chaetotaxy of the genus.Crossref | GoogleScholarGoogle Scholar |
Cipola, N. G., de Morais, J. W., and Bellini, B. C. (2017). The discovery of Lepidocyrtoides Schött, 1917 (Collembola, Entomobryidae, Entomobryinae) from the New World, including three new species from Brazil and one from Australia. Zootaxa 4324, 201–248.
| The discovery of Lepidocyrtoides Schött, 1917 (Collembola, Entomobryidae, Entomobryinae) from the New World, including three new species from Brazil and one from Australia.Crossref | GoogleScholarGoogle Scholar |
Cipola, N. G., de Morais, J. W., and Bellini, B. C. (2018a). New species, redescriptions and a new combination of Acanthocyrtus Handschin, 1925 and Amazhomidia Cipola & Bellini, 2016 (Collembola, Entomobryidae, Entomobryinae). Zootaxa 4387, 401–435.
| New species, redescriptions and a new combination of Acanthocyrtus Handschin, 1925 and Amazhomidia Cipola & Bellini, 2016 (Collembola, Entomobryidae, Entomobryinae).Crossref | GoogleScholarGoogle Scholar | 29690473PubMed |
Cipola, N. G., Arbea, J., Baquero, E., Jordana, R., de Morais, J. W., and Bellini, B. C. (2018b). The survey of Seira Lubbock, 1870 (Collembola, Entomobryidae, Seirinae) from Iberian Peninsula and Canary Islands, including three new species. Zootaxa 4458, 1–66.
| The survey of Seira Lubbock, 1870 (Collembola, Entomobryidae, Seirinae) from Iberian Peninsula and Canary Islands, including three new species.Crossref | GoogleScholarGoogle Scholar | 30314142PubMed |
Cipola, N. G., de Morais, J. W., and Bellini, B. C. (2019a). New subgenus and four species of Lepidocyrtus Bourlet (Collembola, Entomobryidae, Lepidocyrtinae) from Amazon. Insect Systematics & Evolution 50, 189–234.
| New subgenus and four species of Lepidocyrtus Bourlet (Collembola, Entomobryidae, Lepidocyrtinae) from Amazon.Crossref | GoogleScholarGoogle Scholar |
Cipola, N. G., de Morais, J. W., Godeiro, N. N., and Bellini, B. C. (2019b). Taxonomic revision of Brazilian genus Tyrannoseira Bellini & Zeppelini, 2011 (Collembola, Entomobryidae, Seirinae). Zootaxa 4586, 201–248.
| Taxonomic revision of Brazilian genus Tyrannoseira Bellini & Zeppelini, 2011 (Collembola, Entomobryidae, Seirinae).Crossref | GoogleScholarGoogle Scholar |
D’Aguilar, J., and Raimbault, F. (1990). Notes de bibliographye entomologique. Entomologiste 46, 37–40.
Deharveng, L., Jantarit, S., and Bedos, A. (2018). Revisiting Lepidonella Yosii (Collembola: Paronellidae): character overview, checklist of world species and reassessment of Pseudoparonella doveri Carpenter. Annales de la Société entomologique de France (N.S.) 54, 381–400.
| Revisiting Lepidonella Yosii (Collembola: Paronellidae): character overview, checklist of world species and reassessment of Pseudoparonella doveri Carpenter.Crossref | GoogleScholarGoogle Scholar |
Delamare-Deboutteville, C. (1948). Recherches sur les Collemboles termitophiles et myrmécophiles (ecologie, ethologie, systematique). Archives de Zoologie Expérimentale et Générale 85, 261–425.
Ding, Y. H., and Zhang, F. (2015). Contribution to the eyed Sinella from China: two new species and additional reports on nine known species (Collembola: Entomobryidae). Zootaxa 3973, 474–490.
| Contribution to the eyed Sinella from China: two new species and additional reports on nine known species (Collembola: Entomobryidae).Crossref | GoogleScholarGoogle Scholar | 26249872PubMed |
Fjellberg, A. (1999). The labial palp in Collembola. Zoologischer Anzeiger 237, 309–330.
Fjellberg, A. (2007). The Collembola of Fennoscandia and Denmark. Part II: Entomobryomorpha and Symphypleona. Fauna Entomologia Scandinavica 42, 1–264.
| The Collembola of Fennoscandia and Denmark. Part II: Entomobryomorpha and Symphypleona.Crossref | GoogleScholarGoogle Scholar |
Fourcroy, A. F. (1785). ‘Entomologia Parisiensis; sive catalogus insectorum quæ in agro Parisiensi reperiuntur; secundam methodam Geoffrœanam in sectiones, genera & species distributus: cui addita sunt nomina trivialia & fere trecentæ novæ species.’ pp. 232–544. (Pars secunda. Parisiis.)
Geoffroy, E. L. (1762). ‘Histoire abrégée des Insectes qui se trouvent aux environs de Paris.’ Tome second. (Durand: Paris.)
Gisin, H. (1944). Materialen zur Revision der Collembolen. Bulletin de la Société Entomologique Suisse 19, 121–156.
Gisin, H. (1963). Collemboles d’Europe V. Revue Suisse de Zoologie 7, 77–101.
Gisin, H. (1964a). Collemboles d’Europe VI. Revue Suisse de Zoologie 71, 383–400.
| Collemboles d’Europe VI.Crossref | GoogleScholarGoogle Scholar |
Gisin, H. (1964b). Collemboles d’Europe VII. Revue Suisse de Zoologie 71, 649–678.
Gisin, H. (1965). Nouvelles notes taxonomiques sur les Lepidocyrtus. Revue d’Écologie et de Biologie du Sol 2, 519–524.
Gisin, H. (1967). Espèces nouvelles et lignées évolutives de Pseudosinella endogés (Collembola). Memórias e estudos do Museu zoológico da Universidade de Coimbra 301, 6–25.
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposyum Series 41, 95–98.
Hopkin, S. P. (1997). ‘Biology of the Springtails (Insecta: Collembola).’ (Oxford University Press: Oxford, UK.)
Hopkin, S. P. (2007). ‘A Key to the Collembola (springtails) of Britain and Ireland.’ (Field Studies Council.)
Hüther, W. (1986). New aspects in taxonomy of Lepidocyrtus (Collembola). In ‘2nd International Seminar on Apterygota’, 4–6 September 1986, Siena, Italy. (Ed. R. Dallai.) pp. 61-65. (University of Siena: Siena, Italy.)
Jantarit, S., Satasook, Ch., and Deharveng, L. (2014). Cyphoderus (Cyphoderidae) as a major component of collembolan cave fauna in Thailand, with description of two new species. ZooKeys 368, 1–21.
| Cyphoderus (Cyphoderidae) as a major component of collembolan cave fauna in Thailand, with description of two new species.Crossref | GoogleScholarGoogle Scholar |
Jantarit, S., Satasook, Ch., and Deharveng, L. (2019). Coecobrya sirindhornae sp. n., the most highly troglomorphic Collembola in southeast Asia (Collembola, Entomobryidae). ZooKeys 824, 21–44.
| Coecobrya sirindhornae sp. n., the most highly troglomorphic Collembola in southeast Asia (Collembola, Entomobryidae).Crossref | GoogleScholarGoogle Scholar |
Katoh, K., Rozewicki, J., and Yamada, K. D. (2019). MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20, 1160–1166.
| MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization.Crossref | GoogleScholarGoogle Scholar | 28968734PubMed |
Katz, A. D., Giordano, R., and Soto-Adames, F. (2015). Taxonomic review and phylogenetic analysis of fifteen North American Entomobrya (Collembola, Entomobryidae), including four new species. ZooKeys 525, 1–75.
| Taxonomic review and phylogenetic analysis of fifteen North American Entomobrya (Collembola, Entomobryidae), including four new species.Crossref | GoogleScholarGoogle Scholar |
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., and Calcott, B. (2017). Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
| 28013191PubMed |
Letunic, I., and Bork, P. (2019). Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Research 47, W256–W259.
| Interactive Tree Of Life (iTOL) v4: recent updates and new developments.Crossref | GoogleScholarGoogle Scholar | 30931475PubMed |
Lubbock, J. (1873). ‘Monograph of the Collembola and Thysanura.’ (The Ray Society: London, UK.)
Lukić, M., Porco, D., Bedos, A., and Deharveng, L. (2015). The puzzling distribution of Heteromurus (Verhoeffiella) absoloni Kseneman, 1938 (Collembola: Entomobryidae: Heteromurinae) resolved: detailed redescription of the nominal species and description of a new species from Catalonia (Spain). Zootaxa 4039, 249–275.
| The puzzling distribution of Heteromurus (Verhoeffiella) absoloni Kseneman, 1938 (Collembola: Entomobryidae: Heteromurinae) resolved: detailed redescription of the nominal species and description of a new species from Catalonia (Spain).Crossref | GoogleScholarGoogle Scholar | 26624478PubMed |
Lukić, M., Delić, T., Zagmajster, M., and Deharveng, L. (2018). Setting a morphological framework for the genus Verhoeffiella (Collembola, Entomobryidae) for describing new troglomorphic species from the Dinaric karst (western Balkans). Invertebrate Systematics 32, 1118–1170.
| Setting a morphological framework for the genus Verhoeffiella (Collembola, Entomobryidae) for describing new troglomorphic species from the Dinaric karst (western Balkans).Crossref | GoogleScholarGoogle Scholar |
Ma, Y., and Shi, S. (2018). Three new species of Entomobrya (Collembola: Entomobryidae) from China. European Journal of Taxonomy 419, 1–21.
| Three new species of Entomobrya (Collembola: Entomobryidae) from China.Crossref | GoogleScholarGoogle Scholar |
Mari Mutt, J. A. (1986). Puerto Rican species of Lepidocyrtus and Pseudosinella (Collembola: Entomobryidae). Caribbean Journal of Science 22, 1–48.
Mateos, E. (2008a). The European Lepidocyrtus Bourlet, 1839 (Collembola: Entomobryidae). Zootaxa 1769, 35–59.
| The European Lepidocyrtus Bourlet, 1839 (Collembola: Entomobryidae).Crossref | GoogleScholarGoogle Scholar |
Mateos, E. (2008b). Definition of Lepidocyrtus lusitanicus Gama, 1964 species-complex (Collembola, Entomobryidae), with description of new species and color forms from the Iberian Peninsula. Zootaxa 1917, 38–54.
| Definition of Lepidocyrtus lusitanicus Gama, 1964 species-complex (Collembola, Entomobryidae), with description of new species and color forms from the Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |
Mateos, E. (2011). New Lepidocyrtus Bourlet, 1839 taxa from Greece (Collembola: Entomobryidae). Zootaxa 3108, 25–40.
| New Lepidocyrtus Bourlet, 1839 taxa from Greece (Collembola: Entomobryidae).Crossref | GoogleScholarGoogle Scholar |
Mateos, E. (2012). The European Lepidocyrtus lanuginosus group (Collembola: Entomobryidae), definition and description of a new species from Spain. Zootaxa 3570, 69–81.
| The European Lepidocyrtus lanuginosus group (Collembola: Entomobryidae), definition and description of a new species from Spain.Crossref | GoogleScholarGoogle Scholar |
Mateos, E., and Greenslade, P. (2015). Towards understanding Lepidocyrtus Bourlet, 1839 (Collembola, Entomobryidae) I: diagnosis of the subgenus Setogaster, new records and redescriptions of species. Zootaxa 4044, 105–129.
| Towards understanding Lepidocyrtus Bourlet, 1839 (Collembola, Entomobryidae) I: diagnosis of the subgenus Setogaster, new records and redescriptions of species.Crossref | GoogleScholarGoogle Scholar | 26624705PubMed |
Mateos, E., and Petersen, H. (2012). Definition of the European Lepidocyrtus curvicollis group (Collembola: Entomobryidae) with description of a new species from Sardinia (Italy). Zootaxa 3273, 51–62.
| Definition of the European Lepidocyrtus curvicollis group (Collembola: Entomobryidae) with description of a new species from Sardinia (Italy).Crossref | GoogleScholarGoogle Scholar |
Mateos, E., and Winkler, D. (2018). New data clarifying the taxonomy of European members of the Lepidocyrtus pallidus–serbicus group (Collembola, Entomobryidae). Zootaxa 4429, 548–568.
| New data clarifying the taxonomy of European members of the Lepidocyrtus pallidus–serbicus group (Collembola, Entomobryidae).Crossref | GoogleScholarGoogle Scholar | 30313256PubMed |
Mateos, E., Escuer, P., Busmachiu, G., Riutort, M., and Álvarez-Presas, M. (2018). Untangling Lepidocyrtus (Collembola, Entomobryidae): new molecular data shed light on the relationships of the European groups. Invertebrate Systematics 32, 639–651.
| Untangling Lepidocyrtus (Collembola, Entomobryidae): new molecular data shed light on the relationships of the European groups.Crossref | GoogleScholarGoogle Scholar |
Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop’, 14 November 2010, New Orleans, LA, USA. INSPEC Accession number 11705685. (IEEE.)
Minh, B. Q., Nguyen, M. A. T., and Von Haeseler, A. (2013). Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30, 1188–1195.
| Ultrafast approximation for phylogenetic bootstrap.Crossref | GoogleScholarGoogle Scholar | 23418397PubMed |
Nguyen, L. T., Schmidt, H. A., Von Haeseler, A., and Minh, B. Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268–274.
| IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.Crossref | GoogleScholarGoogle Scholar | 25371430PubMed |
Nilsai, A., Jantarit, S., Satasook, C., and Zhang, F. (2017). Three new species of Coecobrya (Collembola: Entomobryidae) from caves in the Thai peninsula. Zootaxa 4286, 187–202.
| Three new species of Coecobrya (Collembola: Entomobryidae) from caves in the Thai peninsula.Crossref | GoogleScholarGoogle Scholar |
Nunes, R. D., and Bellini, B. C. (2018). Three new species of Entomobryoidea (Collembola: Entomobryomorpha) from Brazilian Caatinga-Cerrado transition, with identification keys to Brazilian Cyphoderus, Pseudosinella and Trogolaphysa species. Zootaxa 4420, 71–96.
| Three new species of Entomobryoidea (Collembola: Entomobryomorpha) from Brazilian Caatinga-Cerrado transition, with identification keys to Brazilian Cyphoderus, Pseudosinella and Trogolaphysa species.Crossref | GoogleScholarGoogle Scholar |
Pan, Z. X., Zhang, F., and Li, Y. B. (2015). Two closely related Homidia species (Entomobryidae, Collembola) revealed by morphological and molecular evidence. Zootaxa 3918, 285–294.
| Two closely related Homidia species (Entomobryidae, Collembola) revealed by morphological and molecular evidence.Crossref | GoogleScholarGoogle Scholar | 25781095PubMed |
Parfitt, E. (1891). Devon Collembola and Thysanura. Report and Transactions of the Devonshire Association for the Advancement of Science Literature and Art 23, 322–352.
Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
| ABGD, Automatic Barcode Gap Discovery for primary species delimitation.Crossref | GoogleScholarGoogle Scholar | 21883587PubMed |
Ren, Y., Li, Z., and Zhang, F. (2018). A new species of Dicranocentrus Schött from Hainan (China) with a key to the Chinese species of the genus (Collembola, Entomobryidae). ZooKeys 762, 59–68.
| A new species of Dicranocentrus Schött from Hainan (China) with a key to the Chinese species of the genus (Collembola, Entomobryidae).Crossref | GoogleScholarGoogle Scholar |
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |
Santos, I. P. S., Cipola, N. G., de Morais, J. W., and Bellini, B. C. (2016). A new species of Campylothorax (Collembola: Paronellidae: Paronellinae) from northern Brazil. Zoologia 33, 1–6.
| A new species of Campylothorax (Collembola: Paronellidae: Paronellinae) from northern Brazil.Crossref | GoogleScholarGoogle Scholar |
Snider, R. J. (1967). The chaetotaxy of North American Lepidocyrtus s. str. (Collembola: Entomobryidae). Contributions of the American Entomological Institute 2, 1–28.
Soto-Adames, F. N. (2010). Two new species and descriptive notes for five Pseudosinella species (Hexapoda: Collembola: Entomobryidae) from West Virginian (USA) caves. Zootaxa 2331, 1–34.
Szeptycki, A. (1967). Morpho-systematic studies on Collembola. Part 1. Materials to a revision of the genus Lepidocyrtus Bourlet, 1839 (Entomobryidae s.l.). Acta Zoologica CracoviensIa 12, 369–377.
Szeptycki, A. (1972). Morpho-systematic studies on Collembola III. Body chaetotaxy in the first instars of several genera of the Entomobryomorpha. Acta Zoologica Cracoviensia 17, 341–372.
Szeptycki, A. (1979). ‘Chaetotaxy of the Entomobryidae and its Phylogenetical Significance. Morpho-systematic Studies of Collembola, IV.’ (Polska Akademia Nauk, Zakład Zoologii Systematycznej i Doświadczalnej: Kraków, Poland.)
Talavera, G., and Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.
| Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.Crossref | GoogleScholarGoogle Scholar | 17654362PubMed |
Wang, F., Chen, J. X., and Christiansen, K. (2003). Taxonomy of the genus Lepidocyrtus s.l. (Collembola: Entomobryidae) in East and Southeast Asia and Malaysia, with description of a new species from the People’s Republic of China. Canadian Entomologist 135, 823–837.
| Taxonomy of the genus Lepidocyrtus s.l. (Collembola: Entomobryidae) in East and Southeast Asia and Malaysia, with description of a new species from the People’s Republic of China.Crossref | GoogleScholarGoogle Scholar |
Winkler, D. (2016). A new species of Lepidocyrtus (Collembola, Entomobryidae) from the Börzsöny Mountains, Hungary. Zootaxa 4150, 388–400.
| A new species of Lepidocyrtus (Collembola, Entomobryidae) from the Börzsöny Mountains, Hungary.Crossref | GoogleScholarGoogle Scholar | 27615681PubMed |
Winkler, D. (2017). New Lepidocyrtus Bourlet, 1839 from riverine woodland in Hungary (Collembola, Entomobryidae). Zootaxa 4250, 529–540.
| New Lepidocyrtus Bourlet, 1839 from riverine woodland in Hungary (Collembola, Entomobryidae).Crossref | GoogleScholarGoogle Scholar | 28609993PubMed |
Winkler, D., and Dányi, L. (2017). Redescription of Seira pallidipes Reuter, 1895 and its synonymization with Seira pillichi Stach, 1930 (Collembola, Entomobryidae, Seirini). Zootaxa 4312, 497–514.
| Redescription of Seira pallidipes Reuter, 1895 and its synonymization with Seira pillichi Stach, 1930 (Collembola, Entomobryidae, Seirini).Crossref | GoogleScholarGoogle Scholar |
Winkler, D., and Mateos, E. (2018). Redescription of Lepidocyrtus peisonis Traser & Christian, 1992 with notes on Lepidocyrtus mariani Traser & Dányi, 2008 (Collembola: Entomobryidae). Zootaxa 4375, 392–408.
| Redescription of Lepidocyrtus peisonis Traser & Christian, 1992 with notes on Lepidocyrtus mariani Traser & Dányi, 2008 (Collembola: Entomobryidae).Crossref | GoogleScholarGoogle Scholar | 29690078PubMed |
Winkler, D., and Traser, G. N. (2012). Explanation of the European Lepidocyrtus pallidus–serbicus group (Collembola, Entomobryidae), with description of new species from Hungary. Zootaxa 3394, 35–47.
| Explanation of the European Lepidocyrtus pallidus–serbicus group (Collembola, Entomobryidae), with description of new species from Hungary.Crossref | GoogleScholarGoogle Scholar |
Yosii, R. (1959). Studies on the Collembolan fauna of Malay and Singapore with special reference to the genera: Lobella, Lepidocyrtus and Callyntrura. Contributions from the Biological Laboratory, Kyoto University 10, 1–65.
Yu, D., Zhang, F., and Deharveng, L. (2014). A peculiar cave species of Tomocerus (Collembola, Tomoceridae, Tomocerinae) from Vietnam, with a discussion of the postantennal organ and prelabral chaetae in Tomocerinae. ZooKeys 408, 61–70.
| A peculiar cave species of Tomocerus (Collembola, Tomoceridae, Tomocerinae) from Vietnam, with a discussion of the postantennal organ and prelabral chaetae in Tomocerinae.Crossref | GoogleScholarGoogle Scholar |
Zhang, F., and Dong, R. R. (2014). Three new species of Coecobrya (Collembola: Entomobryidae) from southern and northwest China. Zootaxa 3760, 260–274.
| Three new species of Coecobrya (Collembola: Entomobryidae) from southern and northwest China.Crossref | GoogleScholarGoogle Scholar | 24870081PubMed |
Zhang, B., Chen, T. W., Mateos, E., Scheu, S., and Schaefer, I. (2018a). Cryptic species in Lepidocyrtus lanuginosus (Collembola: Entomobryidae) are sorted by habitat type. Pedobiologia 68, 12–19.
| Cryptic species in Lepidocyrtus lanuginosus (Collembola: Entomobryidae) are sorted by habitat type.Crossref | GoogleScholarGoogle Scholar |
Zhang, F., Jantarit, S., Nilsai, A., Stevens, M. I., Ding, Y., and Satasook, C. (2018b). Species delimitation in the morphologically conserved Coecobrya (Collembola: Entomobryidae): a case study integrating morphology and molecular traits to advance current taxonomy. Zoologica Scripta 47, 342–356.
| Species delimitation in the morphologically conserved Coecobrya (Collembola: Entomobryidae): a case study integrating morphology and molecular traits to advance current taxonomy.Crossref | GoogleScholarGoogle Scholar |
Zhang, B., Chen, T. W., Mateos, E., Scheu, S., and Schaefer, I. (2019a). DNA-based approaches uncover cryptic diversity in the European Lepidocyrtus lanuginosus species group (Collembola: Entomobryidae). Invertebrate Systematics 2019, 661–670.
| DNA-based approaches uncover cryptic diversity in the European Lepidocyrtus lanuginosus species group (Collembola: Entomobryidae).Crossref | GoogleScholarGoogle Scholar |
Zhang, F., Bellini, B. C., and Soto-Adames, F. N. (2019b). New insights into the systematics of Entomobryoidea (Collembola: Entomobryomorpha): first instar chaetotaxy, homology and classification. Zoological Systematics 44, 249–278.