Four decades of multidisciplinary studies on isopods: a tribute to Pavel Ličar

Authors

  • Urban Bogataj
  • Damjana Drobne
  • Anita Jemec
  • Rok Kostanjšek
  • Polona Mrak
  • Sara Novak
  • Simona Prevorčnik
  • Boris Sket
  • Peter Trontelj
  • Magda Tušek Žnidarič
  • Miloš Vittori
  • Primož Zidar
  • Nada Žnidaršič
  • Jasna Štrus

DOI:

https://doi.org/10.14720/abs.59.2.15854

Keywords:

isopods, terrestrial, aquatic, functional morphology, developmental biology, host-microbiota interactions, terrestrial isopod, aquatic isopod, ecotoxicology, systematics, evolution

Abstract

In this paper we review the research on aquatic and terrestrial isopods during the last four decades at the Chair of Zoology, Department of Biology, Biotech- nical Faculty, University of Ljubljana. Isopods have attracted substantial attention from our research team in the followingareas: functional morphology and developmental biology, host-microbiota specific interactions, ecotoxicology, and systematics and evolution. We present the rationale for using two isopod species as our central model organisms: the waterlouse (Asellus aquaticus) and thewoodlouse (Porcellio scaber). We summarize the most important and interesting findings about the structure and function of the integument and digestive systems of several amphibious and terrestrial woodlice species during molting and developmental stages, the importance of P. scaber as a model organism in the study of arthropod-microbe interactions, and its central role as a test model in terrestrial ecotoxicity studies. We highlight the role that A. aquaticus has played in studying the evolution of subterranean biodiversity and in the evolution of troglomorphies. Inaddition to the retrospective view on our research with isopods we also present the scope of our future research, and the importance for zoology(biology). We wish to dedicate this work to our late co-worker, Prof. Dr. Pavel Ličar, who devoted much of his research into studying the digestive system of freshwater asellids (Isopoda: Asellota).

References

Alwes, F. and Scholtz, G., 2014. The early development of the onychopod cladoceran Bythotrephes longimanus (Crustacea, Branchiopoda). Frontiers in Zoology, 11(1), p.1. DOI: https://doi.org/10.1186/1742-9994-11-10

Argano, R., 1979. Isopodi (Crustacea: Isopoda). Guide per il riconoscimento delle specie animali delle acque interne Italiane 5, 1–65.

Beeby, A., 1978. Interaction of lead and calcium uptake by the woodlouse, Porcellio scaber (Isopoda, Porcellionidae). Oecologia, 32(2), 255-262. DOI: https://doi.org/10.1007/BF00366076

Bibič, A., Drobne, D., Štrus, J., Byrne, A.R., 1997. Assimilation of zinc by Porcellio scaber (Isopoda, Crustacea) exposed to zinc. Bulletin of Environmental Contamination and Toxicology, 58(5), 814-821. DOI: https://doi.org/10.1007/s001289900407

Birštejn, J. A., 1951. Presovodnye osliki (Asellota). In Pavlovskii, E. N. & Štakelyberg, A. A. (Eds.), Fauna SSSR, Rakoobraznye, 7. Akademii Nauk SSSR, Moscou, pp. 144

Bourtzis, K. and Miller, T.A., 2003. Insect symbiosis. CRC Press, Boca Raton, FL. DOI: https://doi.org/10.1201/9780203009918

Browne, W.E., Price, A.L., Gerberding, M., Patel, N.H., 2005. Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis. Genesis, 42(3), 124-149. DOI: https://doi.org/10.1002/gene.20145

Corsaro, D. and Venditti, D., 2004. Emerging chlamydial infections. Critical Reviews in Microbiology, 30(2), 75-106. DOI: https://doi.org/10.1080/10408410490435106

Dallinger, R. and Prosi, F., 1988. Heavy metals in the terrestrial isopod Porcellio scaber Latreille. II. Subcellular fractionation of metal-accumulating lysosomes from hepatopancreas. Cell Biology and Toxicology, 4(1), 97-109. DOI: https://doi.org/10.1007/BF00141289

Donker, M.H., Koevoets, P., Verkleij, J.A. and Van Straalen, N.M., 1990. Metal binding compounds in hepatopancreas and haemolymph of Porcellio scaber (Isopoda) from contaminated and re- ference areas. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 97(1), 119-126. DOI: https://doi.org/10.1016/0742-8413(90)90181-8

Drobne, D., 1995. Bacteria adherent to the hindgut of terrestrial isopods. Acta Microbiologica et Immunologica Hungarica, 42(1), 45-52.

Drobne, D., 1997. Terrestrial isopods—a good choice for toxicity testing of pollutants in the terrestrial environment. Environmental Toxicology and Chemistry, 16(6), 1159-1164. DOI: https://doi.org/10.1002/etc.5620160610

Drobne, D. Ličar, Rode J., 1991a. Morfološka analiza želodca pri vrstah Titanethes albus, Ligidium hypnorum in Hyloniscus sp. (Isopoda, Crustacea) in njeni filogenetski vidiki = Functional morphology of the stomach in Titanethes albus, Ligidium hypnorum and Hyloniscus sp. (Isopoda, Crustacea) and its phylogenetic aspects. Biološki vestnik 39 (3), 1–10.

Drobne, D., Ličar, P., Štrus, J., Drašlar, K., 1991b. A comparative study on the morphology of the stomach in terrestrial isopods (Oniscoidea, Isopoda). V: Kurzfassungen der Vorträge und Poster. [s.l.]: Zoologisches Institut der Universität Heidelberg, pp. 19.

Drobne, D. and Hopkin, S.P., 1994. Ecotoxicological laboratory test for assessing the effects of chemi- cals on terrestrial isopods. Bulletin of Environmental Contamination and toxicology, 53(3), 390-397. DOI: https://doi.org/10.1007/BF00197231

Drobne, D. and Hopkin, S.P., 1995. The toxicity of zinc to terrestrial isopods in a” standard” laboratory test. Ecotoxicology and Environmental Safety, 31(1), 1-6. DOI: https://doi.org/10.1006/eesa.1995.1037

Drobne, D. and Štrus, J., 1996. Moult frequency of the isopod Porcellio scaber, as a measure of zinc‐ contaminated food. Environmental Toxicology and Chemistry, 15(2), 126-130. DOI: https://doi.org/10.1002/etc.5620150209

Drobne, D., Štrus, J., Zidar, P., Ličar, P.,1999a. Delovanje organskih sistemov rakov v normalnih in stresnih razmerah in pomen teh spoznanj v ekotoksikologiji. V: 80-letnica biologije na Univerzi v Ljubljani : zbornik povzetkov : Ljubljana, 1. oktober 1999. Ljubljana: Oddelek za biologijo Biotehniške fakultete Univerze v Ljubljani, pp. 12-13

Drobne, D., Štrus, J., Žnidaršič, N. Zidar, P., 1999b. Morphological Description of Bacterial Infection of Digestive Glands in the Terrestrial Isopod Porcellio scaber (Isopoda, Crustacea). Journal of Invertebrate Pathology, 73(1), 113-119. DOI: https://doi.org/10.1006/jipa.1998.4818

Drobne, D., Blažič, M., Van Gestel, C.A., Lešer, V., Zidar, P., Jemec, A., Trebše, P., 2008. Toxicity of imidacloprid to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Chemosphere, 71(7), 1326-1334. DOI: https://doi.org/10.1016/j.chemosphere.2007.11.042

Golobič, M., Jemec, A., Drobne, D., Romih, T., Kasemets, K., Kahru, A., 2012. Upon exposure to Cu nanoparticles, accumulation of copper in the isopod Porcellio scaber is due to the dissolved Cu ions inside the digestive tract. Environmental Science & Technology, 46(21), 12112-12119. DOI: https://doi.org/10.1021/es3022182

Hames, C.A.C. and Hopkin, S.P., 1989. The structure and function of the digestive system of terrestrial isopods. Journal of Zoology, 217(4), 599-627. DOI: https://doi.org/10.1111/j.1469-7998.1989.tb02513.x

Harding, P.T., Sutton, S.L., 1985. Woodlice in Britain and Ireland: distribution and habitat. Institute of Terrestrial Ecology, Huntingdon

Hassall, M., Turner, J.G., Rands, M.R.W., 1987. Effect of terrestrial isopods on the decomposition of woodland leaf litter. Oecologia. 72, 597–604. DOI: https://doi.org/10.1007/BF00378988

Hejnol, A., Schnabel, R., Scholtz, G., 2006. A 4D-microscopic analysis of the germ band in the iso- pod crustacean Porcellio scaber (Malacostraca, Peracarida) - developmental and phylogenetic implications. Development Genes and Evolution, 216, 755-767. DOI: https://doi.org/10.1007/s00427-006-0105-4

Henry, J.P. and Magniez, G., 1983. Introduction pratique à la systématique des organismes des eaux continentales françaises. 4. Crustacés Isopodes (principalement Asellotes). Bulletin de la Societe Linneenne de Lyon, 52, 319-357. DOI: https://doi.org/10.3406/linly.1983.10613

Henry, J.P. and Magniez, G., 1995. Nouvelles données sur les Asellidae épigés d’Extrême-Orient. Contributions to Zoology, 65(2), 101-122. DOI: https://doi.org/10.1163/26660644-06502003

Henry, J. P., Magniez, G., Notenboom, J., 1996. Isopoda Asellota de Turquie recoltés en 1987. Con- tributions to Zoology 66, 55–62. DOI: https://doi.org/10.1163/26660644-06601003

Hopkin, S.P., Hardisty, G.N. and Martin, M.H., 1986. The woodlouse Porcellio scaber as a ‘biological indicator’of zinc, cadmium, lead and copper pollution. Environmental Pollution Series B, Chemical and Physical, 11(4), 271-290. DOI: https://doi.org/10.1016/0143-148X(86)90045-5

Jemec, A., Drobne, D., Remškar, M., Sepčić, K., Tišler, T., 2008. Effects of ingested nano‐sized tita- nium dioxide on terrestrial isopods (Porcellio scaber). Environmental Toxicology and Chemistry, 27(9), 1904-1914. DOI: https://doi.org/10.1897/08-036.1

Jemec, A., Kos, M., Drobne, D., Koponen, I.K., Vukić, J., Ferreira, N.G., Loureiro, S. and McShane, H.V., 2016. In field conditions, commercial pigment grade TiO2 was not harmful to terrestrial isopods but reduced leaf litter fragmentation. The Science of the Total Environment, 571, 1128. DOI: https://doi.org/10.1016/j.scitotenv.2016.07.107

Karaman, S.L., 1952. Asellus aquaticus i njegove podvrste na Balkanu. Prirodoslovni istraživački institut, Jugoslovenska akademija znanosi i umjetnosti, 25, 80–85.

Kaschl, U., Zidar, P., Štrus, J., Storch,V.,2002. Food choice experiments with cadmium nitrate dosed food in terrestrial isopod Oniscus asellus (Crustacea). Acta Biologica Slovenica 45(2), 3-14.

Kolar, L., Jemec, A., van Gestel, C.A., Valant, J., Eržen, N.K. Zidar, P., 2010. Toxicity of abamectin to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Ecotoxicology, 19(5), 917-927. DOI: https://doi.org/10.1007/s10646-010-0473-4

Konec, M., Prevorčnik, S., Sarbu, S.M., Verovnik, R. and Trontelj, P., 2015. Parallels between two geographically and ecologically disparate cave invasions by the same species, Asellus aquaticus (Isopoda, Crustacea). Journal of Evolutionary Biology, 28(4), 864-875. DOI: https://doi.org/10.1111/jeb.12610

Konec, M., Delić, T. and Trontelj, P., 2016. DNA barcoding sheds light on hidden subterranean boundary between Adriatic and Danubian drainage basins. Ecohydrology, 9, 1304–1312. DOI: https://doi.org/10.1002/eco.1727

Kostanjšek, R., Štrus, J., Avgustin, G., 2002. Genetic diversity of bacteria associated with the hindgut of the terrestrial crustacean Porcellio scaber (Crustacea : Isopoda). Fems Microbiology Ecology, 40, 171-179. DOI: https://doi.org/10.1111/j.1574-6941.2002.tb00950.x

Kostanjšek, R., Štrus, J., Drobne, D. and Avguštin, G., 2004. ‘Candidatus Rhabdochlamydia por- cellionis’, an intracellular bacterium from the hepatopancreas of the terrestrial isopod Porcellio scaber (Crustacea: Isopoda). International Journal of Systematic and Evolutionary Microbiology, 54(Pt 2), 543-549. DOI: https://doi.org/10.1099/ijs.0.02802-0

Kostanjšek, R., Štrus, J., Lapanje, A., Avguštin, G., Rupnik, M., Drobne, D., 2006. Intestinal microbiota of terrestrial isopods. In: König, H., Varma A. (eds): Intestinal microorganisms of termites and other invertebrates (Soil Biology 6). Springer, Berlin, Germany, pp. 115–131. DOI: https://doi.org/10.1007/3-540-28185-1_5

Kostanjšek, R., Štrus, J., Avguštin, G., 2007. “Candidatus Bacilloplasma,” a novel lineage of Mollicutes associated with the hindgut wall of the terrestrial isopod Porcellio scaber (Crustacea: Isopoda). Applied and Environmental Microbiology, 73(17), 5566-5573. DOI: https://doi.org/10.1128/AEM.02468-06

Kostanjšek, R., Milatovič, M. and Štrus, J., 2010. Endogenous origin of endo-β-1, 4-glucanase in common woodlouse Porcellio scaber (Crustacea, Isopoda). Journal of Comparative Physiology B, 180(8), 1143-1153. DOI: https://doi.org/10.1007/s00360-010-0485-7

Kostanjšek, R., Marolt, T.P., 2015a. Pathogenesis, tissue distribution and host response to Rhabdo- chlamydia porcellionis infection in rough woodlouse Porcellio scaber. Journal of Invertebrate Pathology, 125, 56-67. DOI: https://doi.org/10.1016/j.jip.2015.01.001

Kostanjšek, R., Vittori, M., Srot, V., Bußmann, B., van Aken, P.V., Štrus, J., 2015b. Phosphate-accumu- lating bacterial community in calcium bodies of isopod crustacean Titanethes albus. In: Abstracts, 12th Multinational Congress on Microscopy, Eger, Hungary, August 23-28, 2015, pp. 430-432.

Lane R.L., 1988. The Digestive System of Porcellio scaber Latreille, 1804 (Isopoda, Oniscoidea): Histology and Histochemistry. Crustaceana, 55(2),113-128. DOI: https://doi.org/10.1163/156854088X00465

Lapanje, A., Drobne, D., Nolde, N., Valant, J., Muscet, B., Leser, V. Rupnik, M., 2008. Long-term Hg pollution induced Hg tolerance in the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Environmental pollution, 153(3),537-547. DOI: https://doi.org/10.1016/j.envpol.2007.09.016

Lešer, V., Drobne, D., Vilhar, B., Kladnik, A., Žnidaršič, N. Štrus, J., 2008. Epithelial thickness and lipid droplets in the hepatopancreas of Porcellio scaber (Crustacea: Isopoda) in different physio- logical conditions. Zoology, 111(6), 419-432. DOI: https://doi.org/10.1016/j.zool.2007.10.007

Ličar, P., 1970. Predhodno poročilo o morfologiji želodca pri družini Asellidae (Isopoda Aquatica). Biološki vestnik, 18, 45-50.

Ličar, P., Sket, B., 1971. Morfologija želodca pri družinah Asellidae in Stenasellidae (Isopoda, Asellota) in njeni filogenetski vidik. Biološki vestnik, 1, 131-138.

Ličar, P., 1976. Morfologija in velikost želodca nekaterih taksonov družine Asellidae (Isopoda, Asel- lota). Biološki vestnik 24 (1), 39-46.

Ličar, P., 1977. The fine structure of filters in the stomach of Asellus aquaticus (Isopoda, Asellota). Slovenska akademija Ljubljana, Dissertationes Classis IV:217–226.

Ličar, P., Blejec, A., Urbanc-Berčič, O., 1979. Mehanske lastnosti primarnega filtra v želodcu pri Asellus aquaticus cavernicolus (Isopoda, Asellota). Biološki vestnik, 1(27),33-48.

Liebmann, H., 1962. Handbuch der Frischwasser- und Abwasser-Biologie, Band I. Oldenbourg, München, pp. 588.

Milatovič, M., Kostanjšek, R., Štrus, J., 2010. Ontogenetic development of Porcellio scaber: Staging based on microscopic anatomy. Journal of Crustacean Biology, 30 (2), 225-235. DOI: https://doi.org/10.1651/09-3189.1

Mittmann, B., Ungerer, P., Klann, M., Stollewerk, A., Wolff, C., 2014. Development and staging of the water flea Daphnia magna (Straus, 1820; Cladocera, Daphniidae) based on morphological landmarks. EvoDevo, 5,12. DOI: https://doi.org/10.1186/2041-9139-5-12

Mrak, P., Žnidaršič, N., Tušek-Žnidarič, M., Klepal, W., Gruber, D., Štrus, J., 2012. Egg envelopes and cuticle renewal in Porcellio embryos and marsupial mancas. Zookeys, 176, 55-72. DOI: https://doi.org/10.3897/zookeys.176.2418

Mrak, P., Žnidaršič, N., Žagar, K., Čeh, M., Štrus, J., 2014. Exoskeletal cuticle differentiation during intramarsupial development of Porcellio scaber (Crustacea: Isopoda). Arthropod Structure and Development, 43, 423-439. DOI: https://doi.org/10.1016/j.asd.2014.07.002

Mrak, P., Bogataj, U., Štrus, J., Žnidaršič, N., 2015. Formation of the hindgut cuticular lining during embryonic development of Porcellio scaber (Crustacea, Isopoda). Zookeys, 515, 93-109. DOI: https://doi.org/10.3897/zookeys.515.9468

Nolde, N., Drobne, D., Valant, J., Padovan, I. Horvat, M., 2006. Lysosomal membrane stability in labo- ratory and field exposed terrestrial isopods Porcellio scaber (Isopoda, Crustacea). Environmental Toxicology and Chemistry, 25(8), 2114-2122. DOI: https://doi.org/10.1897/05-593R1.1

Novak, S., Drobne, D., Valant, J., Pipan‐Tkalec, Ž., Pelicon, P., Vavpetič, P., Grlj, N., Falnoga, I., Mazej, D. and Remškar, M., 2012a. Cell membrane integrity and internalization of ingested TiO2 nanoparticles by digestive gland cells of a terrestrial isopod. Environmental Toxicology and Chemistry, 31(5), 1083-1090. DOI: https://doi.org/10.1002/etc.1791

Novak, S., Drobne, D., Valant, J., Pelicon, P., 2012b. Internalization of consumed TiO2 nanoparticles by a model invertebrate organism. Journal of Nanomaterials, 3. DOI: https://doi.org/10.1155/2012/658752

Novak, S., Drobne, D., Golobič, M., Zupanc, J., Romih, T., Gianoncelli, A., Kiskinova, M., Kaulich, B., Pelicon, P., Vavpetič, P. and Jeromel, L., 2013. Cellular internalization of dissolved cobalt ions from ingested CoFe2O4 nanoparticles: in vivo experimental evidence. Environmental Science & Technology, 47(10), 5400-5408. DOI: https://doi.org/10.1021/es305132g

Prevorčnik, S., Blejec, A. and Sket, B., 2004. Racial differentiation in Asellus aquaticus (L.)(Crustacea: Isopoda: Asellidae). Archiv für Hydrobiologie, 160(2), 193-214. DOI: https://doi.org/10.1127/0003-9136/2004/0160-0193

Protas, M.E., Trontelj, P.,Patel, N.H., 2011. Genetic basis of eye and pigment loss in the cave crusta- cean, Asellus aquaticus. Proceedings of the National Academy of Sciences, 108(14), 5702-5707. DOI: https://doi.org/10.1073/pnas.1013850108

Protas, M. and Jeffery, W.R., 2012. Evolution and development in cave animals: from fish to crusta- ceans. Wiley Interdisciplinary Reviews: Developmental Biology, 1(6), 823-845. DOI: https://doi.org/10.1002/wdev.61

Romih, T., Drašler, B., Jemec, A., Drobne, D., Novak, S., Golobič, M., Makovec, D., Susič, R.,Kogej, K., 2015. Bioavailability of cobalt and iron from citric-acid-adsorbed CoFe 2 O 4 nanoparticles in the terrestrial isopod Porcellio scaber. Science of the Total Environment, 508, 76-84. DOI: https://doi.org/10.1016/j.scitotenv.2014.11.080

Schmalfuss, H., 2003. World catalog of terrestrial isopods (Isopoda: Oniscidea). Staatliches Museum für Naturkunde. Scholtz, G., Ponomarenko, E., Wolf, C., 2009. Cirripede Cleavage Patterns and the Origin of the Rhizocephala (Crustacea: Thecostraca). Arthropod Systematics & Phylogeny, 67 (2), 219-228. DOI: https://doi.org/10.3897/asp.67.e31698

Sixt, B.S., Kostanjšek, R., Mustedanagic, A., Toenshoff, E.R, Horn, M., 2013. Developmental cycle and host interaction of Rhabdochlamydia porcellionis, an intracellular parasite of terrestrial isopods. Environmental Microbiology, 15(11), 2980-2993. DOI: https://doi.org/10.1111/1462-2920.12252

Sket, B., 1994. Distribution of Asellus aquaticus (Crustacea: Isopoda: Asellidae) and its hypogean populations at different geographic scales, with a note on Proasellus istrianus*. Hydrobiologia, 287, 39–47. DOI: https://doi.org/10.1007/BF00006895

Sket, B., 1965a. Taxonomische Problematik der Art Asellus aquaticus (L.) Rac. mit besonderer Rücksicht auf die Populationen Sloweniens. Slovenska akademija znanosti in umetnosti, Razred za prirodoslovne in medicinske vede, Oddelek za prirodoslovne vede. Razprave, 8, 177–221.

Sket, B., 1965b. Subterrane Asellus-Arten Jugoslaviens (Crustacea, Isopoda). Acta Mus. Maced. Sc. Nat., 10(1), 1-25.

Sket B., 1967. Crustacea Isopoda (aquatica). In: Catalogus faunae Jugoslaviae, Cons. Acad. Sc. RPSF Jugoslaviae, 3(3), 1-21.

Stamataki, E., Pavlopoulos, A., 2016. Non-insect crustacean models in developmental genetics including an encomium to Parhyale hawaiensis. Current Opinion in Genetics & Development, 39, 149-156. DOI: https://doi.org/10.1016/j.gde.2016.07.004

Stanek, K., Gabrijelčič, E., Drobne, D., Trebše, P., 2003. Inhibition of acetylcholinesterase activity in the terrestrial isopod Porcellio scaber as a biomarker of organophosphorus compounds in food. Arhiv za higijenu rada i toksikologiju, 54(3), 183-188.

Storch, V., 1987. Microscopic anatomy and ultrastructure of the stomach of Porcellio scaber (Crustacea, Isopoda).Zoomorphology 106, 301. DOI: https://doi.org/10.1007/BF00312004

Storch, V. and Štrus, J., 1989. Microscopic anatomy and ultrastructure of the alimentary canal in terrestrial isopods. Monografia. Monitore Zoologico Italiano 4, 105-126.

Štrus, J., Blejec, A., 1983. Reproductive activity in Asellus aquaticus (Crustacea, Isopoda) from Ljubljansko barje = Razmnoževanje vodnega oslička Asellus aquaticus (Crustacea, Isopoda) z Ljubljanskega barja. Biološki vestnik, 2, 83-92.

Štrus J, Burkhardt P, Storch V., 1985 The ultrastructure of the midgut glands in Ligia italica under different nutritional conditions. Helgol. Wiss. Meeresunters, 39,367–374. DOI: https://doi.org/10.1007/BF01987408

Štrus J., Drobne, D., Ličar, P., 1995. Comparative anatomy and functional aspects of the digestive system in amphibious and terrestrial isopods (Isopoda: Oniscoidea). V: Alikhan, M.A. (Ed.:). Terrestrial Isopod Biology. Rotterdam: A. A. Balkema, 9, 15-23.

Štrus J., Blejec A., 2001. Microscopic anatomy of the integument and digestive system during the molt cycle in Ligia italica (Oniscidea). In: Kensley, B., Brusca, R.C. (Eds.). Crustacean Issues 13, Isopod Systematics and Evolution, pp. 343-352.

Štrus, J. and Storch, V., 2004. Comparative electron microscopic study of the stomach of Orchestia ca- vimana and Arcitalitrus sylvaticus (Crustacea: Amphipoda). Journal of Morphology, 259, 340-346. Štrus J., Klepal W., Repina J., Tusek-Znidaric M., Milatovic M., Pipan Z. 2008. Ultrastructure of the digestive system and the fate of midgut during embryonic development in Porcellio scaber (Crustacea: Isopoda). Arthropod Struct. Dev., 37(4), 287-98. DOI: https://doi.org/10.1016/j.asd.2007.11.004

Turk, S., Sket, B. and Sarbu, Ş., 1996. Comparison between some epigean and hypogean populations of Asellus aquaticus (Crustacea: Isopoda: Asellidae). Hydrobiologia, 337(1-3), 161-170. DOI: https://doi.org/10.1007/BF00028517

Turk-Prevorčnik, S., Blejec, A., 1998. Asellus aquaticus infernus, new subspecies (Isopoda: Asellota: Asellidae), from Romanian hypogean waters. Journal of Crustacean Biology, 18, 763–773. DOI: https://doi.org/10.1163/193724098X00647

Valant, J. and Drobne, D., 2012. Biological reactivity of TiO2 nanoparticles assessed by ex vivo testing. Protoplasma, 249(3), 835-842. DOI: https://doi.org/10.1007/s00709-011-0298-x

Van Gestel, C.A.M., 2012. Soil ecotoxicology: state of the art and future directions. Zookeys, 176, 275–296. DOI: https://doi.org/10.3897/zookeys.176.2275

Verovnik, R., Sket, B., Prevorčnik, S., Trontelj, P., 2003. Random amplified polymorphic DNA di- versity among surface and subterranean populations of Asellus aquaticus (Crustacea: Isopoda). Genetica, 119(2), 155-165. DOI: https://doi.org/10.1023/A:1026085716777

Verovnik, R., Sket, B., Trontelj, P., 2004. Phylogeography of subterranean and surface populations of water lice Asellus aquaticus (Crustacea: Isopoda). Molecular Ecology, 13(6), 1519-1532. DOI: https://doi.org/10.1111/j.1365-294X.2004.02171.x

Verovnik, R., Sket, B., Trontelj, P., 2005. The colonization of Europe by the freshwater crustacean Asellus aquaticus (Crustacea: Isopoda) proceeded from ancient refugia and was directed by habitat connectivity. Molecular Ecology, 14(14), 4355-4369. DOI: https://doi.org/10.1111/j.1365-294X.2005.02745.x

Verovnik, R., Prevorčnik, S., Jugovic, J., 2009. Description of a neotype for Asellus aquaticus Linné, 1758 (Crustacea: Isopoda: Asellidae), with description of a new subterranean Asellus species from Europe. Zoologischer Anzeiger-A Journal of Comparative Zoology, 248(2), 101-118. DOI: https://doi.org/10.1016/j.jcz.2009.03.001

Vittori, M., Žnidaršič, N., Žagar, K., Čeh, M., Štrus, J., 2012. Calcium bodies of Titanethes albus (Crustacea: Isopoda): Molt-related structural dynamics and calcified matrix-associated bacteria. Journal of Structural Biology, 180(1), 216-225. DOI: https://doi.org/10.1016/j.jsb.2012.05.014

Vittori, M., Rozman, A., Grdadolnik, J., Novak, U., Štrus, J., 2013. Mineral Deposition in Bacteria- Filled and Bacteria-Free Calcium Bodies in the Crustacean Hyloniscus riparius (Isopoda: Oni- scidea). PloS one, 8(3), 1-14. DOI: https://doi.org/10.1371/journal.pone.0058968

Vittori, M. and Štrus, J., 2014. The integument in troglobitic and epigean woodlice (Isopoda: Onisci- dea): a comparative ultrastructural study. Zoomorphology, 133(4), 391-403. DOI: https://doi.org/10.1007/s00435-014-0232-9

Williams, W.D., 1962, The geographical distribution of the isopods Asellus aquaticus (L.) and A. meridianus Rac. In Proceedings of the Zoological Society of London, 139, 75-96. Blackwell Publishing Ltd. DOI: https://doi.org/10.1111/j.1469-7998.1962.tb01823.x

Zidar, P., Drobne, D., Štrus, J., 1998. Determination of moult stages of Porcellio scaber (Isopoda) for routine use. Crustaceana, 71, 646-654. DOI: https://doi.org/10.1163/156854098X00644

Zidar, P., Drobne, D., Štrus, J., Blejec, A., 2003. Intake and assimilation of zinc, copper, and cadmium in the terrestrial isopod Porcellio scaber Latr.(Crustacea, Isopoda). Bulletin of Environmental Contamination and Toxicology, 70(5), 1028-1035. DOI: https://doi.org/10.1007/s00128-003-0086-1

Zidar, P., Drobne, D., Štrus, J., Van Gestel, C.A.M., Donker, M., 2004. Food selection as a means of Cu intake reduction in the terrestrial isopod Porcellio scaber (Crustacea, Isopoda). Applied Soil Ecology, 25(3), 257-265. DOI: https://doi.org/10.1016/j.apsoil.2003.09.005

Zidar, P., Božič, J., Štrus, J., 2005. Behavioral response in the terrestrial isopod Porcellio scaber (Crustacea) offered a choice of uncontaminated and cadmium-contaminated food. Ecotoxicology, 14(5), 493-502. DOI: https://doi.org/10.1007/s10646-005-0005-9

Zidar, P., Hribar, M., Žižek, S. and Štrus, J., 2012. Behavioural response of terrestrial isopods (Cru- stacea: Isopoda) to pyrethrins in soil or food. European Journal of Soil Biology, 51,51-55. DOI: https://doi.org/10.1016/j.ejsobi.2012.03.010

Zimmer, M., 2002. Nutrition in terrestrial isopods (Isopoda : Oniscidea): an evolutionary-ecological approach. Biological Reviews, 77, 455-493. DOI: https://doi.org/10.1017/S1464793102005912

Žižek, S. and Zidar, P., 2013. Toxicity of the ionophore antibiotic lasalocid to soil-dwelling inverte- brates: Avoidance tests in comparison to classic sublethal tests. Chemosphere, 92(5), 570-575. DOI: https://doi.org/10.1016/j.chemosphere.2013.04.007

Žnidaršič, N., Štrus, J, Drobne, D., 2003. Ultrastructural alterations of the hepatopancreas in Porcellio scaber under stress. Environmental Toxicology and Pharmacology, 13(3), 161-174. DOI: https://doi.org/10.1016/S1382-6689(02)00158-8

Žnidaršič, N., Tušek-Žnidarič, M., Falnoga, I., Ščančar, J., Štrus, J., 2005. Metallothionein-like proteins and zinc-copper interaction in the hindgut of Porcellio scaber (Crustacea: Isopoda) exposed to zinc. Biological Trace Element Research, 106(3), 253-264. DOI: https://doi.org/10.1385/BTER:106:3:253

Žnidaršič, N., Matsko, N., Tušek-Žnidarič, M., Letofsky-Papst, I., Grogger, W., Hofer, F., Štrus, J., 2010. Architecture of the Crustacean Cuticle: Imaging of Mineralized Organic Matrix by LM, TEM and AFM. Imaging & Microscopy, 3, 23-25.

Žnidaršič, N., Mrak, P., Tušek-Žnidarič, M., Štrus, J., 2012. Exoskeleton anchoring to tendon cells and muscles in molting isopod crustaceans. Zookeys, 176, 39-53. DOI: https://doi.org/10.3897/zookeys.176.2445

Downloads

Published

01.12.2016

How to Cite

Bogataj, U., Drobne, D., Jemec, A., Kostanjšek, R., Mrak, P., Novak, S., Prevorčnik, S., Sket, B., Trontelj, P., Tušek Žnidarič, M., Vittori, M., Zidar, P., Žnidaršič, N., & Štrus, J. (2016). Four decades of multidisciplinary studies on isopods: a tribute to Pavel Ličar. Acta Biologica Slovenica, 59(2), 5-25. https://doi.org/10.14720/abs.59.2.15854

Similar Articles

1-10 of 93

You may also start an advanced similarity search for this article.