100 years of research on the Protura: many secrets still retained
Keywords:
Hexapoda, Apterygota, Ellipura, Nonoculata, history of researchAbstract
The Protura were discovered relatively late in the history of entomology. The first description of these minute soil arthropods was given in 1907 by the Italian entomologist Filippo Silvestri, who named them ‘Protura’. Shortly thereafter his fellow countryman Antonio Berlese published two brief notes on these animals before his grand monograph of the ‘Myrientomata’, as he named them, appeared in 1909.
The centennial of the discovery of Protura offers the opportunity to review our knowledge about these peculiar animals. In the end, we must confess that proturans continue to retain an amazing number of secrets, including basic facts of knowledge about their biology and ecology. Up to the present, they have concealed from scientific observation their sexual life and the mode of sperm transmission. For a long time, their egg deposition and early development were completely obscure topics; only recently has it become possible to conduct first observations on their embryology. The list of open questions can be easily extended: we know only little about their nutritional biology, and next to nothing about their sensory systems, communication, physiological and ecological capacities.
The greatest progress in proturan research over the past 100 years has been made in the field of taxonomy. Nonetheless, the road of taxonomy was bumpy and the proturans proved to be awkward travel companions. Species are exceedingly difficult to determine; and the number of living scientists that are able to unambiguously identify specimens at the species level can be counted on two hands. Proturans inhabit soils in all terrestrial regions of the earth (excepting the Arctic and Antarctic regions). Presently, a total of 787 valid species has been described. Because of the high standards of Berlese’s 1909 monograph, several decades would pass before morphological and anatomical research could equal or go beyond his classical landmark. In more recent times, remarkable contributions have been made to the ultrastructural investigation of internal organs and sperm morphology; hereby, the proturans proved again to be odd and unusual in many respects. The peculiarities of Protura have evoked heated debates about their phylogenetic position from the beginning, and such discussions have recently been revived by the introduction of molecular data. The review comprehends an extensive reference list on all research topics except taxonomy, which recently was compiled by Szeptycki (2007).
Downloads
References
Alberti, G., Kratzmann, M., Blaszak, C. & A. Szeptycki (1989): Reaktion von Mikroarthropoden auf Waldkalkungen. – Mitteilungen der Deutschen Gesellschaft für allgemeine und angewandte Entomologie 7: 119–122.
Aubertot, M. M. (1939): Présence d’un vaisseau dorsal contractile chez les Protoures du genre Acerentomon. – Comptes Rendus hebdomadaíres des Séances de l’Académie des Sciences, Paris 208: 120–122.
Ax, P. (1999): Das System der Metazoa II. Ein Lehrbuch der Phylogenetischen Systematik. – Fischer, Stuttgart: 384 pp.
Baccetti, B., Dallai, R. & B. Fratello (1973): The “12 + 0”, “14 + 0” or aflagellate sperm of Protura. – Journal of Cell Science 13: 321–335.
Balkenhol, B. (1996): Activity range and dispersal of the Protura Acerentomon nemorale (Arthropoda: Insecta). – Pedobiologia 40: 212–216.
Bedini, C. & P. Tongiorgi (1971): The fine structure of the pseudoculus of Acerentomids Protura (Insecta, Apterygota). – Monitore zoologico italiano (n. s.) 5: 25–38.
Berlese, A. (1905): Apparecchio per raccogliere presto ed in gran numero piccoli Artropodi. – Redia 2: 85–90.
Berlese, A. (1908a): Nuovi Acerentomidi. – Redia, 5: 16–19.
Berlese, A. (1908b): Osservazioni intorno agli Acerentomidi. Nota preventiva. – Redia, 5: 110–122. Berlese, A. (1909): Monografia dei Myrientomata. – Redia 6: 1–182. Pls I–XVII.
Bernard, E. C. (1976): Observations on the eggs of Eosentomon australicum (Protura: Eosentomidae). – Transactions of the American Microscopical Society 95: 129–130.
Bernard, E. C. (1979): Egg types and hatching of Eosentomon Berlese (Protura: Eosentomidae). – Transactions of the American Microscopical Society 98: 123–126.
Bernard, E. C. (1990): New species, clarifications, and changes in status within Eosentomon Berlese (Hexapoda: Protura: Eosentomidae) from the United States. – Proceedings of the Biological Society of Washington 103: 861–890.
Bernard, E. C. (1996): Aggressive proturan: Eosentomon rostratum and Acerentulus confinis. – http:// eppserver.ag.utk.edu/Class/EPP555/Aggressive_Proturan.avi. Accessed 2 October 2009.
Biliniski, S. (1977): Oogenesis in Acerentomon gallicum Jonescu (Protura). Previtellogenic and vitellogenic stages. – Cell Tissue Research 179: 401–412.
Bilinski S. & J. Klag (1977): The oogenesis in Acerentomon gallicum Jonescu (Protura). An ultrastructural analysis of chorion formation. – Acta Biologica Cracoviensia Series Zoologia 20: 101–106.
Bilinski S. & J. Klag (1979): The ultrastructure of midgut cells in Acerentomon gallicum Jonescu (Protura). – Folia Biolologica (Krakow) 27: 3–7.
Bitsch, C. & J. Bitsch (1998): Internal anatomy and phylogenetic relationships among apterygote insect clades (Hexapoda). – Annales de la Société Entomologique de France (N. S.) 34: 339–363.
Bitsch, C. & J. Bitsch (2000): The phylogenetic interrelationships of the higher taxa of apterygote hexapods. – Zoologica Scripta 29: 131–156.
Bitsch, C. & J. Bitsch (2004): Phylogenetic relationships of basal hexapods among the mandibulate arthropods: a cladistic analysis based on comparative morphological characters. – Zoologica Scripta 33: 511–550.
Böhm, A., D. Bartel, N. U. Szucsich & G. Pass (2011): Confocal imaging of the exo- and endoskeleton of Protura after non-destructive DNA extraction. – Soil Organisms 83(3): 335–345.
Börner, C. (1910): Die phylogenetische Bedeutung der Protura. – Biologisches Centralblatt 30: 633–641. Boudreaux, H. B. (1987): Arthropod phylogeny, with special reference to insects. Robert E. Krieger Publishing Company, Malabar Florida: 320 pp.
Brusca, R. C. & G. J. Brusca (1990): Invertebrates. Sinauer Associates, Sunderland, Massachusetts: 922 pp. Capurro, M., Galli, L. & C. Torti (2009): Protura of Liguria (NW Italy). – Acta Zoologica Cracoviensia Ser. B – Invertebrata 52: 45–56.
Carapelli, A., F. Frati, F. Nardi, R. Dallai & C. Simon (2000): Molecular phylogeny of the apterygotan insects based on nuclear and mitochondrial genes. – Pedobiologia 44: 361–373.
Chen, W.-J., Y. Bu, A. Carapelli, R. Dallai, S. Li, W.-Y. Yin, Y.-X. Luan (2011): The mitochondrial genome of Sinentomon erythranum (Arthropoda: Hexapoda: Protura): an example of highly divergent evolution. – BMC Evolutionary Biology 11(1): 246–258.
Christian, E. & A. Szeptycki (2004): Distribution of Protura along an urban gradient in Vienna. – Pedobiologia 48: 445–452.
Condé, B. (1945): Contribution à la faune française des Protoures. Revue française d’Entomologie 12: 99–115.
Condé, B. & J. François (1962): Prèsence de glandes tégumentaires unicellulaires chez les Protoures. – Bulletin de la Société Zoologique de France 87: 221–225.
Dallai, R. (1976): Fine structure of the pyloric region and Malpighian papillae of Protura (Insecta Apterygota). – Journal of Morphology 150: 727–762.
Dallai, R. (1977a): Comparative analysis of the hindgut in two species of Protura (Insecta, Apterygota). – Journal of Morphology 151: 165–186.
Dallai, R. (1977b): Fine structure of Protura intestine. – Revue d´Ecologie et de Biologie du Sol 24: 139–152.
Dallai, R. (1978): The pyloric region of Collembola and Protura. – In: Dallai, R. (ed): Proceedings of the 3rd International Seminar on Apterygota – University of Siena, Siena: 175–177.
Dallai, R. (1991): Are Protura really Insects? – In: Simonetta, A. M. & S. C. Morris (eds): The early evolution of Metazoa and the significance of problematic taxa. Cambridge University Press, Cambridge: 263–269.
Dallai, R. & D. Burroni (1981): La struttura delle ghiandole tegumentali delle zampe anteriori dei Proturi (Insecta). – Redia, 64: 165–172.
Dallai, R. & J. François (1986): Fine structure of the proturan hypopharyngeal sensilla. – In: Dallai, R. (ed.) 2nd International Seminar on Apterygota, Siena: 287–293.
Dallai, R. & J. Nosek (1980): Fine structure of tarsal sensory organs in the forelegs of proturan Acerentomon. – Proceedings of the 16th International Congress of Entomology Kyoto 1980: 41.
Dallai, R. & J. Nosek (1981): Ultrastructure of sensillum t1 on foretarsus of Acerentomon maius Berlese (Protura, Acerentomidae) – International Journal of Insect Morphology and Embryology 10: 321–330.
Dallai, R. & W.-Y. Yin (1983): Sperm structure of Sinentomon (Protura) and phylogenetic considerations. – Pedobiologia 25: 313–316.
Dallai, R., P. Lupetti & C. Mencarelli (2006): Unusual axonemes of hexapod spermatozoa. – International Review of Cytology 254: 45–99.
Dallai, R., L. Xué & W.-Y. Yin (1990). Aflagellated spermatozoa of Huhentomon and Acerella (Protura: Apterygota). – International Journal of Insect Morphology and Embryology 19: 211–217.
Dallai, R., L. Xué & W.-Y. Yin (1992): Flagellate spermatozoa of Protura (Insecta, Apterygota) are motile. – International Journal of Insect Morphology and Embryology 21: 137–148.
Dallai, R., W.-Y. Yin, L. Z. Xué & P. P. Fanciulli (1987). Fine structure of the pyloric region and of the hindgut in the proturan Neocondeellum dolichotarsum (Insecta, Protura). – Journal of Morphology 194: 173–86.
Dallai, R., W.-Y. Yin, L. Z. Xué & J. François (1989): The gut structure of Sinentomon erythranum Yin (Protura: Sinentomidae). – International Journal of Insect Morphology and Embryology 18: 173–184.
Dallai, R., D. Mercati, Y. Bu, W.-Y. Yin, G. Callaini & M. G. Riparbelli (2010a): The spermatogenesis and sperm structure of Acerentomon microrhinus (Protura, Hexapoda) with considerations on the phylogenetic position of the taxon. – Zoomorphology 129: 61–80.
Dallai, R., D. Mercati, Y. Bu & W.-Y. Yin (2010b): Spermatogenesis and sperm structure of Acerella muscorum (Ionescu, 1930) (Hexapoda, Protura). – Tissue & Cell 42: 97–104.
Dell’Ampio, E., N. U. Szucsich, A. Carapelli, F. Frati, G. Steiner, A. Steinacher & G. Pass (2009): Testing for misleading effects in the phylogenetic reconstruction of ancient lineages of hexapods: influence of character dependence and character choice in analyses of 28S rRNA sequences. – Zoologica Scripta 38: 155–170.
Dell’Ampio, E., N. U. Szucsich & G. Pass (2011): Protura and molecular phylogenetics: status quo of a young love. – Soil Organisms 83(3): 347–358.
Denis, J. R. (1949): Protoures. – Traité de Zoologie, Vol. 9.– Masson, Paris: 186–207.
Ewing, H. E. (1936): Synonymy and synopsis of the genera of the order Protura. – Proceedings of the Biological Society of Washington 49: 159–166.
Ewing, H. E. (1940): The Protura of North America. – Annals of the Entomological Society of America, Columbus 33: 495–541.
François, J. (1959): Squelette et musculature cephaliques d’ Acerentomon propinquum (Condé) (Ins. Protoures). – Travaux du Laboratoire de Zoologie et de la Station aquicole Grimaldi de la Faculté des Sciences de Dijon 29: 57 pp.
François, J. (1960): Développement postembryonnaire d’un protoure du genre Acerentomon SILV. – Travaux du Laboratoire de Zoologie et de la Station aquicole Grimaldi de la Faculté des Sciences de Dijon 33: 1–14.
François, J. (1964): Le squelette thoracique des Protoures. – Travaux du Laboratoire de Zoologie et de la Station aquicole Grimaldi de la Faculté des Sciences de Dijon 55: 1–18.
François, J. (1965): Sur la presence de glandes neuroendocrines retrocrebrales chez les Protoures (Insectes Apterygotes). – Comptes Rendus de l’Académie des Sciences, Paris 260: 2307–2309.
François, J. (1969): Anatomie et morphologie céphalique des protoures (Insecta Apterygota). – Mémoires du Muséum national d’Histoire naturelle, Paris (N. S.), ser. A, 49: 1–144.
François, J. (1996): Squelette et musculature thoracique des Protoures. – Annales de la Société entomologique de France (N. S.), 32: 233–249.
François, J. (2003a): Analyse cladistique de l’ordre des Protoures (Hexapoda, Protura). – Bulletin de la Société entomologique de France 108: 109–125.
François, J. (2003b): Ultrastructure du cœur d’Acerentomon affine Bagnall (Prot., Acerentomidae). – Bulletin de la Société entomologique de France 108: 263–264.
François, J. (2006): Analyse cladistique du genre Acerentomon Silvestri, 1907 (Protura, Acerentomidae). – Bulletin de la Société entomologique de France 111: 5–10.
François, J. & R. Dallai (1986a): Ultrastructure des glandes maxillaires d’Acerentomon affine Badn. et d’Eosentomon transitorium Berl. (Apterygota: Protura). – International Journal of Insect Morphology and Embryology 15: 201–212.
François, J. & R. Dallai (1986b): Les glandes abdominales des Protoures. – In: Dallai, R. (ed): Proceedings of the 2nd International Seminar on Apterygota, Siena: 273–280.
François, J. & R. Dallai (1989): Anatomie et morphologie de l’appareil genital male des protoures (Apterygota). – Annales de la Société entomologique de France (N. S.) 25: 121–133.
François, J., Dallai, R. & W.-Y. Yin (1992): Cephalic anatomy of Sinentomon erythranum Yin (Protura: Sinentomidae). – International Journal of Insect Morphology and Embryology 21: 199–213.
Fukui, M. & R. Machida (2006): Embryonic development of Baculentulus densus (Imadaté): its outline (Hexapoda: Protura, Acerentomidae). – Proceedings of the Arthropodan Embryological Society Japan 41: 21–28.
Gao, Y., Y. Bu & Y. Luan (2008): Phylogenetic Relationships of Basal Hexapods Reconstructed from Nearly Complete 18S and 28S rRNA gene Sequences. – Zoological Science 25: 1139–1145.
Giribet, G., G. D. Edgecombe, J. M. Carpenter, C. A. D’Haese & W. C. Wheeler (2004): Is Ellipura monophyletic? A combined analysis of basal hexapod relationships with emphasis on the origin of insects. – Organisms, Diversity & Evolution 4: 319–340.
Giribet, G., S. Richter, G. D. Edgecombe & W. C. Wheeler (2005): The position of crustaceans within Arthropoda - evidence from nine molecular loci and morphology. – In: Koenemann, S. & R. A. Jenner (eds): Crustacea and Arthropod Relationships: Crustacean Issues 16: – Festschrift for F. R. Schram. Taylor & Francis, Boca Raton: 307–352.
Gunnarsson, B. (1980): Distribution, abundance and population structure of Protura in two woodland soils in Southwestern. Sweden. – Pedobiologia 20: 254–262.
Hågvar, S. (1984): Effects of liming and artificial acid rain on Collembola and Protura in coniferous forest. – Pedobiologia 27: 341–354.
Haarløv, N. (1960): Microarthropods from Danish Soils: Ecology, Phenology. – Oikos Supplement 3: 1–176.
Handschin, E. (1929): Urinsekten oder Apterygota (Protura, Collembola, Diplura und Thysanura). – In: F. Dahl (ed): Tierwelt Deutschlands und der angrenzenden Meeresteile. Fischer, Jena, 16: I–VI: 150 pp.
Hansen, J. (2006): Proturan vs. springtail. http://eppserver.ag.utk.edu/Class/EPP555/Protura.mov. Accessed 2 October 2009
Hansen, J. A., Bernard, E. C. & J. K. Moulton (2010): A defensive behaviour of Acerentulus confinis (Berlese) (Protura, Acerentomidae). – Proceedings of the Entomological Society of Washington 112: 43–46.
Haupt, J. (1972a): Kutikula-Strukturen der Pseudoculi von Pauropoden und Proturen. – Naturwissenschaften 59: 80.
Haupt, J. (1972b): Ultrastruktur des Pseudoculus von Eosentomon (Protura, Insecta). – Zeitschrift für Zellforschung 135: 539–551.
Hennig, W. (1953): Kritische Bemerkungen zum phylogenetischen System der Insekten. – Beiträge zur Entomologie, Sonderheft 3, 85 pp.
Hennig, W. (1969): Die Stammesgeschichte der Insekten. – Kramer, Frankfurt am Main: 436 pp.
Hickman, C. P., L. S. Roberts, S. Keen, A. Larson & H. l’Anson (2011): Integrated Principles of Zoology. 15th ed. – McGraw-Hill, New York: 842 pp.
Imadaté, G. (1966): Taxonomic arrangement of Japanese Protura (IV). The proturan chaetotaxy and its meaning to phylogeny. – Bulletin of the National Science Museum, Tokyo 9: 277–315.
Imadaté, G. (1973): Habitat segregation between proturan species. – Zeitschrift für Zoologische Systematik und Evolutionsforschung 11: 287–303.
Imadaté, G. (1974): Protura (Insecta). – Tokyo, Keigaku Publishing Co.: 351 pp.
Imadaté, G. (1977): Occurrence of Sinentomon (Protura) in Japan. – Bulletin of the National Science Museum, Tokyo (Zoology) 3: 37–48.
Imadaté, G. (1980): The prelarva of Nipponentomon nippon (Yoshii) (Protura, Acerentomidae). – Annotationes Zoologicae Japonenses 53: 46–49.
Imadaté, G. (1981): Brief accounts of proturan fauna of Japan. I. Frequency distribution of acerentomid species in Hokkaido, Kyushu and the Ryukyu Islands. – Edaphologia 23: 29–36.
Janetscheck, H. (1970): Protura. – In: Helmcke, J.-G., D. Starck & H. Wermuth (eds): Handbuch der Zoologie. de Gruyter, Berlin, Vol. 4: 1–73.
Jura, C. (1975): Ovaries structure in Acerentomon dispar Stach (Protura). – Acta Biologica Cracoviensia Series Zoologia 18: 55–65.
Kjer, K. M. (2004): Aligned 18S and Insect Phylogeny. – Systematic Biology 53:506–514.
Klag, J. (1978): Oogenesis in Acerentomon gallicum Jonescu (Protura). An ultrastructural analysis of the early previtellogenic stages. – Cell & Tissue Research 189, 365–374.
Klag, J. & S. Bilinski (1984): Ovaries of Protura are meroistic: ultrastructural studies. – Cytobios 39: 183–189.
Koenemann, S., R. A. Jenner, M. Hoenemann, T. Stemme & B. M. von Reumont (2010): Arthropod phylogeny revisited, with a focus on crustacean relationships. – Arthropod Structure & Development 39: 88–110.
Krauß, J. & W. Funke (1999): Extraordinary high density of Protura in a windfall area of young spruce plants. – Pedobiologia 43: 44–46.
Kristensen, N. P. (1975): The phylogeny of hexapod “orders’’. A critical review of recent accounts. – Zeitschrift für Zoologische Systematik und Evolutionsforschung 13: 1–44.
Kristensen, N. P. (1981): Phylogeny of insect orders. – Annual Review of Entomology 26: 135–157. Kristensen, N. P. (1991): Phylogeny of extant hexapods. – In: Naumann, I. D., P. B. Carne, J. F. Lawrence, E. S. Nielsen, J. P. Spradberry, R. W. Taylor, M. J. Whitten & M. J. Littlejohn (eds): The Insects of Australia, A Textbook for Students and Research Workers. – CSIRO, Melbourne University Press, Melbourne: 125–140.
Kristensen, N. P. (1997): The groundplan and basal diversification of the hexapods. – In: Fortey, R. A. & R. H. Thomas (eds): Arthropod relationships. Systematic Association, Ser 55. – Chapman and Hall, London: 282–293.
Kurihara, Y., T. Shirouzu, S. Tokumasu & S. Harayama (2009): Hirsutella proturicola sp. nov. isolated from a proturan, Baculentulus densus (Protura, Hexapoda). – Mycoscience 50: 56–62.
Larink, O. & S. M. Bilinski (1989): Fine structure of the egg envelopes of one proturan and two collembolan genera (Apterygota). – International Journal of Insect Morphology and Embryology 18: 39–45.
Luan, Y., Y. Zhang, Q. Yue, J. Pang, R. Xie & W. Yin (2003): Ribosomal DNA gene and phylogenetic relationships of Diplura and lower hexapods. – Science in China (Series C) 46: 67–76.
Luan, Y., Y. Yao, R. Xie, Y. Yang, Y. Zhang & W. Yin (2004): Analysis of 18S rRNA gene of Octostigma sinensis (Projapygoidea:Octostigmatidae) supports the monophyly of Diplura. – Pedobiologia 48: 453–459.
Luan, Y., J. M. Mallatt, R. Xié, Y. Yang & W.-Y. Yin (2005) The phylogenetic position of three basal hexapod groups (Protura, Diplura and Collembola) based on ribosomal RNA gene sequences. Molecular Biology and Evolution 22: 1579–1592.
Machida, R. & I. Takahashi (2003): Embryonic development of a proturan Baculentulus densus (Imadaté): Reference to some developmental stages (Hexapoda: Protura, Acerentomidae). – Proceedings of the Arthropod Embryological Society of Japan 38: 13–17.
Machida, R. & I. Takahashi (2004): Rearing technique for proturans (Hexapoda: Protura). – Pedobiologia 48: 227–229.
Machida, R. (2006): Evidence from embryology for reconstructing the relationships of hexapod basal clades. – Arthropod Systematics & Phylogeny 64: 95–104.
Mallatt, J. M. & G. Giribet (2006): Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. – Molecular Phylogenetics and Evolution 40: 772– 794.
Mallatt, J. M., C. W. Craig & M. J. Yoder (2010): Nearly complete rRNA genes assembled from across the metazoan animals: Effects of more taxa, a structure-based alignment, and paired-sites evolutionary models on phylogeny reconstruction. – Molecular Phylogenetics and Evolution 55: 1–17.
Malmström, A. (2008): Temperature tolerance in soil microarthropods:Simulation of forest-fire heating in the laboratory. – Pedobiologia 51: 419–426.
Malmström, A. (2010): The importance of measuring fire severity - Evidence from microarthropod studies. – Forest Ecology and Management 260: 62–70.
Malmström, A., T. Persson, K. Ahlstrom, K. Gongalsky & J. Bengtsson (2009): Dynamics of soil meso- and macrofauna during a 5-year period after clear-cut burning in a boreal forest. – Applied Soil Ecology 43: 61–74.
Malmström, A. & T. Persson (2011) Responses of Collembola and Protura to tree girdling – some support for ectomycorrhizal feeding. – Soil Organisms 83(2): 279–285.
Manton, S. M. (1979): Functional morphology and the evolution of the hexapod classes. – In: Gupta, A. P. (ed): Arthropod Phylogeny. – Van Nostrand, New York: 387–466.
Meusemann, K., B. M. von Reumont, S. Simon, F. Roeding, S. Strauss, P. Kück, I. Ebersberger, M. Walzl, G. Pass, S. Breuers, V. Achter, A. von Haeseler, T. Burmester, H. Hadrys, J. W. Wägele & B. Misof (2010): A phylogenomic approach to resolve the arthropod tree of life. – Molecular Biology and Evolution 27: 2451–2464.
Minor, M. A. (2008): Protura in native and exotic forests in the North Island of New Zealand. – New Zealand Journal of Zoology 35: 271–279.
Mizushima, H. (2004): Feeding preference among four fungal species by Nipponentomon nippon
(Protura: Nipponentomidae). – Japanese Journal of Entomology 7: 69–71.
Müller, H. (1976): Feinbau der Sensillen an den Vorderbeinen der Proturen. – Zoologischer Anzeiger 197: 151–178.
Nakamura, O. & Y. Hagiwara (2006): Proturan communities under three different vegetations in adjacent area. – Bulletin of the Saitama Museum of Natural History 23: 17–22.
Neuherz, H. (1974): Der erste Höhlenfund einer Proture (Insecta, Apterygota) in Österreich. – Höhle, 25: 25–30.
Neuherz, H. (1975): Die Landfauna der Lurgrotte (Teil I). – Sitzungsberichte der österreichischen Akademie der Wissenschaften (Mathem. – naturw. Kl.) 183: 159–285.
Nosek, J. & M. Lichard (1962): Beitrag zur Kenntnis der Vogelnestfauna. – Biologické Práce 8: 29–51.
Nosek, J. (1973): The European Protura. Their taxonomy, ecology and distribution. With keys for determination. – Muséum d’Histoire naturelle, Genève, 345 pp.
Nosek, J. (1975): Niches of Protura in biogeocoenoses. – Pedobiologia 15: 290–298.
Nosek, J. & S. O. Vysotskaya (1976): Study of Protura from the nests of small mammals of Transkarpathian region. – Entomologicheskoe Obozrenie 55: 808–812.
Nosek, J. (1977): Proturan synusies and niche separation in the soil. – Ecological Bulletins 25: 138–142. Paclt, J. (1956): Biologie der primär flügellosen Insekten. VEB Gustav Fischer Verlag, Jena, 258 pp.
Paoli, G. (1928): Antonio Berlese. – Memoire della Società Entomologica Italiana 6: 55–84.
Poggi, R. (2009): Agostino Dodero (1864–1937). Appunti per una biografia. In: Bottelli F., P. M. Giachino (eds.): Contributo alle conoscenze naturalistiche della Valle Oropa (Biella, Italia). Mem. Ass. Nat. Piem., Volume 11: 75–82.
Prell, H. (1911): Über den Tracheenverlauf bei Eosentomidae. – Zoologischer Anzeiger 38: 185–193. Prell, H. (1912): Beiträge zur Kenntnis der Proturen. III. Gliederung und eigne Muskulatur der Beine von Acerentomon und Eosentomon. – Zoologischer Anzeiger 40: 33–50.
Prell, H. (1913): Das Chitinskelett von Eosentomon, ein Beitrag zur Morphologie des Insektenkörpers. – Zoologica, Stuttgart 28: 727–138.
Price, D. W. (1960): A new family of Protura from California. – Annals of the Entomological Society of America 53: 675–678.
Raw, F. (1956): The abundance and distribution of Protura in grassland. – Journal of Animal Ecology 25: 15–21.
Rimsky-Korsakow, M. (1911a): Über die Organisation der Protura Silvestri. – Travaux de la Société des Naturalistes de St. Pétersbourg 52: 2–24 (in Russian with condensed German version).
Rimsky-Korsakow, M. (1911b): Über die systematische Stellung der Protura Silvestri. – Zoologischer Anzeiger 36: 164–168.
Rost-Roszkowska, M. M., R. Machida & M. Fukui (2010): The role of cell death in the midgut epithelium in Filientomon takanawanum (Protura). – Tissue and Cell 42: 24–31.
Rusek, J. (1974): Zur Taxonomie einiger Gattungen der Familie Acerentomidae (Insecta, Protura).– Acta Entomologica Bohemoslovaca 71: 260–281.
Sawahata, T. & M. Narimatsu (2005): Ectomycorrhizal mat as a habitat for proturans in a Japanese red pine forest. – Edaphologia 77: 15–17.
Schaller, F. (1971): Indirect sperm transfer by soil arthropods. – Annual Review of Entomology 16: 407–446.
Schepotieff, A. (1909): Studien über niedere Insekten. I. Protapteron indicum n. g. n. sp. – Zoologische Jahrbücher (Systematik), 28: 121–138.
Shao, H., Y. Zhang, R. Xie & W.-Y. Yin (1999): Mitochondrial cytochrome b sequences variation of Protura and molecular systematics of Apterygota. – Chinese Science Bulletin 44: 2031–2036.
Shrubovych, J. & J. Rusek (2010): Sugaentulus andrzeji sp. nov. from Siberia, Russia (Protura: Acerentomidae: Acerentominae) and key to Acerentominae genera. – Zootaxa 2720: 59–68.
Silvestri, F. (1907): Descrizione di un nuovo genere di Insetti Apterigoti, rappresentante di un nuovo ordine. – Bollettino del Laboratorio di zoologia generale e agraria della R. Scuola superiore d’agricoltura in Portici 1: 296–311.
Sixl, W., J. Nosek & H. Waltinger (1974): Sensory hairs and tegument in Protura. – Pedobiologia, 14: 109–112.
Stumpp, J. (1990): Zur Ökologie einheimischer Proturen (Arthropoda: Insecta) in Fichtenforsten. – Zoologische Beiträge, 33: 345–422.
Sturm, H. (1959): Die Nahrung der Proturen. Beobachtungen an Acerentomon doderoi Silv. und Eosentomon transitorium Berl. – Naturwissenschaften, 46: 90–91.
Szeptycki, A. (1980): Polish Protura. I. Genus Acerentomon Silvestri, 1907. – Polskie Pismo entomologiczne 50: 311–392.
Szeptycki, A. (1984): Three new species of Eosentomon Berlese, 1909, from Poland with redescription of
Eosentomon germanicum Prell, 1912 (Protura). – Polskie Pismo entomologiczne 54: 195–213.
Szeptycki, A. (1986): Remarks on the prelarva and postembryonic development of Protura. – In: Dallai, R. (ed): Proceedings of the 2nd International Seminar on Apterygota. – University of Siena, Siena: 243– 248.
Szeptycki, A. (1988): New genera and species of Protura from the Altai Mts. – Acta Zoologica Cracoviensia 31: 297–362.
Szeptycki, A. (1989): Body chaetotaxy of Sinentomon Yin, 1965, Protura, Sinentomidae. – In: Dallai, R. (ed): Proceedings of the 3rd International Seminar on Apterygota. – University of Siena, Siena: 63–67.
Szeptycki, A. (1991): Polish Protura V. Genus Acerentulus Berlese, 1908 (Acerentomidae).– Acta Zoologica Cracoviensia 34: 164.
Szeptycki, A. (2002): The taxonomy of Protura: Present status and future problems. – Pedobiologia 46: 209–214.
Szeptycki, A. (2007): Catalogue of the World Protura. – Acta Zoologica Cracoviensia 50B: 1–210.
Szucsich, N. U. & G. Pass (2008): Incongruent phylogenetic hypotheses and character conflicts in morphology: The root and early branches of the hexapodan tree. – Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie 16: 415–430.
Tichy, H. (1988): A kinematic study of front legs’ movements in walking Protura (Insecta). – Journal of Experimental Zoology 245: 130–136.
Tuxen, S. L. (1931): Monographie der Proturen. I. Morphologie nebst Bemerkungen über Systematik und Ökologie. – Zeitschrift für Morphologie und Ökologie der Tiere, ser. A, 22: 671–720.
Tuxen S. L. (1949): Über den Lebenszyklus und die postembryonale Entwicklung zweier dänischer Proturengattungen. – Kongelige Danske Videnskabernes Selskab, Biologiske Skrifter 6: 1–50.
Tuxen, S. L. (1950): Über ein neues, sehr abweichendes Stadium in der postembryonalen Entwicklung der Proturen. – Proceedings of the 8th International Congress of Entomology, Stockholm 1948: 577–583.
Tuxen, S. L. (1952): Über das sogenannte Tentorium der Proturen. – Transactions of the 9th International Congress of Entomology, Amsterdam: 143–146
Tuxen, S. L. (1960): Ontogenie und Phylogenie bezogen auf die apterygoten Insekten. – Zoologischer Anzeiger 164: 359–363.
Tuxen, S. L. (1961): Die Variabilität einer Proturen-Art (Acerentomon gallicum Ion.) nebst deren postembryonaler Entwicklung. – Zoologischer Anzeiger 167: 58–69.
Tuxen, S. L. (1963): Phylogenetical trends in the Protura. As shown by relationship between recent genera. – Zeitschrift für Zoologische Systematik und Evolutionsforschung 1: 277–310.
Tuxen, S. L. (1964): The Protura. A revision of the species of the world. With keys for determination. – Hermann, Paris, 360 pp.
Tuxen, S. L. (1977): The systematical position of Sinentomon (Insecta, Protura). – Bulletin of the national Science Museum Tokyo, Ser. A, 3: 25–36.
Tuxen, S. L. (1980): Notes on the Silvestridia complex (Insecta, Protura) in Madagascar. – Revue d’Écologie et du Biologie de Sol 17: 437–443. von Reumont, B. M., K. Meusemann, N. U. Szucsich, E. Dell’Ampio, V. Gowri-Shankar, D. Bartel, S. Simon, H. O. Letsch, R. R. Stocsits, Y. Luan, J. W. Wägele, G. Pass, H. Hadrys & B. Misof (2009): Can comprehensive background knowledge be incorporated into substitution models to improve phylogenetic analyses? A case study on major arthropod relationships. – BMC Evolutionary Biology 9: 119.
Willmann, R. (2003): Phylogenese und System der Insekten. – In: Dathe, H. H. (ed): Lehrbuch der Speziellen Zoologie, Bd. I: Wirbellose Tiere, 5. Teil: Insecta. – Spektrum Akademischer Verlag, Heidelberg, Berlin: 1–70.
Xie, Q., X. Tian, Y. Qin & W. Bu (2009): Phylogenetic comparison of local length plasticity of the small subunit of nuclear rDNAs among all Hexapoda orders and the impact of hyper-length-variation on alignment. – Molecular Phylogenetics and Evolution 50: 310–316.
Xué, L. Z. & R. Dallai (1992). Cell junctions in the gut of Protura. – Tissue & Cell 24: 51–59.
Xué, L. Z. & R. Dallai & W.-Y. Yin (1993): Tracheal ultrastructure of Protura (Insecta, Apterygota).– International Journal of Insect Morphology and Embryology 22: 13–23.
Xué, L. Z. & R. Dallai, W.-Y. Yin (1994): Comparative tracheal structures of Apterygota. – Acta Zoologica Fennica 195: 143–149.
Xué, L. Z. & W.-Y. Yin (1989): Further observations on the pseudoculi of Protura. – In: Dallai, R. (ed): Proceedings of the 3rd International Seminar on Apterygota – University of Siena, Siena: 253–263.
Xué, L. Z. & W.-Y. Yin (1990): The ultrastructure of spermatozoa and spermatogenesis in Fujientomon dicestum (Insecta, Protura), with special reference to its significance on phylogeny. – Contributions of the Shanghai Institute of Entomology 8: 125–130.
Xué, L. Z. & W.-Y. Yin (1991): Ultrastructural observation on the pseudoculus in Huhentomon plicatunguis. – Acta Entomologica Sinica 34: 151–154.
Yin, W.-Y. (1965a): Studies on Chinese Protura I. – Acta Entomologica Sinica, Peking 14: 71–92 (In Chinese with English summary).
Yin, W.-Y. (1965b): Studies on Chinese Protura II. – Acta Entomologica Sinica, Peking 14: 186–195 (In Chinese with English summary).
Yin, W.-Y. (1981): On bionomics of Sinentomon (Protura) and its systematic position. – Contributions from Shanghai Institute of Entomology 1981: 162–170.
Yin, W.-Y. (1984): A new idea on phylogeny of Protura with approach to its origin and systematic position. – Scientia Sinica. Series B 27: 149–160.
Yin, W.-Y. (1999): Arthropoda. Protura. – Fauna Sinica. Science Press, Beijing, XI+510 pp. [In Chinese with English summary].
Yin, W.-Y., R. Dallai, L. Z. Xué (1989) Sperm evolution in Protura. In: Dallai R (ed): Proceedings of the 3rd International seminar on Apterygota. – University of Siena, Siena: 195–198.
Yin, W.-Y., D. S. Wu & Y. M. Yang (1985): The ultrastructure of spermatozoon and spermiogenesis in Gracilentulus (Protura: Berberentomidae). – Contributions from Shanghai Institute of Entomology 5: 323–327.
Yin, W.-Y., Xué, L. Z. & B. Tang (1990): On systematic positions of Hesperentomon and Fujientomon in view of the fine structure of spermatozoa and pseudoculi (Protura). – Contributions from Shanghai Institute of Entomology 9: 121–125.
Yin, W.-Y. & L. Z. Xué (1993): Comparative spermatology of Protura and its significance on proturan systematics. – Scientia Sinica (Series B) 36: 575–586.
Yin, W.-Y., L. Z. Xué & B. W. Tang (1986): A comparative study on pseudoculus of Protura. – In: Dallai, R. (ed): Proceedings of the 2nd International Seminar on Apterygota. – University of Siena, Siena: 249–256.
Yin, W.-Y., L. Z. Xué & B. W. Tang (1990): On systematic positions of Hesperentomon and Fujientomon in view of the fine structure of spermatozoa and pseudoculi (Protura). – Contributions from Shanghai Institute of Entomology 9: 121–125 (In Chinese with English summary).
Yin, W.-Y., Y. Yang, L. Z. Xué & R. Dallai (1985): A “13 + 0” axonemal pattern in the spermatozoon of Neocondeellum dolichotarsum (Insecta, Protura). – Journal of Ultrastructructure Research 93: 179–185.
Zhang, Y., Y. Zhang, Y. Luan, Y. Chen & W. Yin (2001): Phylogeny of higher taxa of Hexapoda according to 12sRNA sequences. – Chinese Science Bulletin 46: 840–842.
Downloads
Published
Issue
Section
License
Soil Organisms is committed to fair open access publishing. All articles are available online without publication fees. Articles published from Vol. 96 No. 3 (2024) onwards are licensed under the Creative Commons Attribution 4.0 International (CC BY 4.0) license. Articles published from Vol. 80 No. 1 through Vol. 96 No. 2 are available under the previous terms, allowing non-commercial, private, and scientific use.
