Abstract
The marbled crayfish Procambarus virginalis is a new obligately parthenogenetic species that was detected in the mid-1990s in the German aquarium trade. Since then it has become a popular pet in many countries throughout the world and a valuable laboratory model for a broad range of biological disciplines. Releases have led to the establishment of wild populations in several European countries, Madagascar and probably Japan, making marbled crayfish an interesting paradigm of evolutionarily young and ongoing bioinvasions. This article provides an annotated bibliography of the scientific and popular scientific literature on marbled crayfish from its detection until today. Each reference is assigned to a publication format and one or more biological categories. The content is shortly described and its significance for marbled crayfish research and general biology is assessed. Of the 239 references listed 140 (58.6%) deal primarily with laboratory experiments on the biology of marbled crayfish and the establishment and use of marbled crayfish as a research model, 74 (31.0%) with its biogeography, invasions and ecology and 25 (10.4%) with hobby aquarist issues and the pet trade.
References
Chucholl, C. (2016) Marbled crayfish gaining ground in Europe: The role of the pet trade as invasion pathway. In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: Global Overview. CRC Press, Boca Raton, pp. 83–114.
Chucholl, C. & Pfeiffer, M. (2010) First evidence for an established Marmorkrebs (Decapoda, Astacida, Cambaridae) population in Southwestern Germany, in syntopic occurrence with Orconectes limosus (Rafinesque, 1817). Aquatic Invasions, 5, 405–412.
https://doi.org/10.3391/ai.2010.5.4.10Chucholl, C., Morawetz, K. & Groß, H. (2012) The clones are coming – strong increase in Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] records from Europe. Aquatic Invasions, 7, 511–519.
https://doi.org/10.3391/ai.2012.7.4.008Fabritius-Vilpoux, K., Bisch-Knaden, S. & Harzsch, S. (2008) Engrailed-like immunoreactivity in the embryonic ventral nerve cord of the Marbled Crayfish (Marmorkrebs). Invertebrate Neuroscience, 8, 177–197.
https://doi.org/10.1007/s10158-008-0081-7Farca Luna, A.J., Hurtado-Zavala, J.I., Reischig, T. & Heinrich, R. (2009) Circadian regulation of agonistic behavior in groups of parthenogenetic marbled crayfish, Procambarus sp. Journal of Biological Rhythms, 24, 64–72.
https://doi.org/10.1177/0748730408328933
Farca Luna, A.J., Heinrich, R. & Reischig, T. (2010) The circadian biology of the marbled crayfish. Frontiers in Bioscience (Elite Edition), 2, 1414–1431.
Faulkes, Z. (2016) Marble crayfish as a new model organism and a new threat to native crayfish conservation. In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: A Global Overview. CRC Press, Boca Raton, pp. 31–53.
Gutekunst, G., Andriantsoa, R., Falckenhayn, C., Hanna, K., Stein, W., Rasamy, J. & Lyko, F. (2018) Clonal genome evolution and rapid invasive spread of the marbled crayfish. Nature Ecology and Evolution, 2, 567–573.
https://doi.org/10.1038/s41559-018-0467-9Jirikowski, G., Kreissl, S., Richter, S. & Wolff, C. (2010) Muscle development in the marbled crayfish – insights from an emerging model organism (Crustacea, Malacostraca, Decapoda). Development, Genes and Evolution, 220, 89–105.
https://doi.org/10.1007/s00427-010-0331-7Jones, J.P.G., Rasamy, J.R., Harvey, A., Toon, A., Oidtmann, B., Randrianarison, M.H., Raminosoa, N. & Ravoahangimalala, O.R. (2009) The perfect invader: A parthenogenic crayfish poses a new threat to Madagascar’s freshwater biodiversity. Biological Invasions, 11, 1475–1482.
https://doi.org/10.1007/s10530-008-9334-yKaldre, K., Haugjärv, K., Liiva, M. & Gross, R. (2015) The effect of two different feeds on growth, carapace colour, maturation and mortality in marbled crayfish (Procambarus fallax f. virginalis). Aquaculture International, 23, 185–194.
https://doi.org/10.1007/s10499-014-9807-1
Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.) (2016) Freshwater Crayfish: A Global Overview. CRC Press, Boca Raton, 702 pp.
Kouba, A., Tíkal, J., Císař, P., Veselý, L., Fořt, M., Příborský, J., Patoka, J. & Buřič, M. (2016) The significance of droughts for hyporheic dwellers: Evidence from freshwater crayfish. Scientific Reports, 6, 26569.
https://doi.org/10.1038/srep26569Lipták, B., Mrugała, A., Pekárik, L., Mutkovič, A., Grul'a, D., Petrusek, A. & Kouba, A. (2016) Expansion of the marbled crayfish in Slovakia: Beginning of an invasion in the Danube catchment? Journal of Limnology, 75, 305–312.
https://doi.org/10.4081/jlimnol.2016.1313
Lukhaup, C. (2001) Procambarus sp. – Der Marmorkrebs. Aquaristik Aktuell, 7+8, 48–51.
Lyko, F. (2017) The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa, 4363 (4), 544–552.
https://doi.org/10.11646/zootaxa.4363.4.6Marten, M., Werth, C. & Marten, D. (2004) Der Marmorkrebs (Cambaridae, Decapoda) in Deutschland – ein weiteres Neozoon im Rheineinzugsgebiet. Lauterbornia, 50, 17–23.
Martin, P., Kohlmann, K. & Scholtz, G. (2007) The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring. Naturwissenschaften, 94, 843–846.
https://doi.org/10.1007/s00114-007-0260-0Martin, P., Thonagel, S. & Scholtz, G. (2016) The parthenogenetic Marmorkrebs (Malacostraca: Decapoda: Cambaridae) is a triploid organism. Journal of Zoological Systematics and Evolutionary Research, 54, 13–21.
https://doi.org/10.1111/jzs.12114Rieger, V. & Harzsch, S. (2008) Embryonic development of the histaminergic system in the ventral nerve cord of the Marbled Crayfish (Marmorkrebs). Tissue and Cell, 40, 113–126.
https://doi.org/10.1016/j.tice.2007.10.004Rubach, M., Crum, S. & Van den Brink, P. (2011) Variability in the dynamics of mortality and immobility responses of freshwater arthropods exposed to chlorpyrifos. Archives of Environmental Contamination and Toxicology, 60, 708–721. https://doi.org/10.1007/s00244-010-9582-6
Scholtz, G. (2016) Happy birthday! The first decade of Marmorkrebs research results and perspectives. In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: A Global Overview. CRC Press, Boca Raton, pp. 3–12.
Scholtz, G., Braband, A., Tolley, L., Reimann, A., Mittmann, B., Lukhaup, C., Steuerwald, F. & Vogt, G. (2003) Parthenogenesis in an outsider crayfish. Nature, 421, 806.
https://doi.org/10.1038/421806aScholz, S., Richter, S. & Wirkner, C.S. (2018) Constant morphological patterns in the hemolymph vascular system of crayfish (Crustacea, Decapoda). Arthropod Structure and Development. [In press]
Seitz, R. (2001) Lebensdaten und Reproduktionsbiologie des Marmorkrebses (Crustacea, Decapoda). Diplomarbeit. Experimentelle Tierökologie, Universität Ulm, Ulm, 55 pp.
Seitz, R., Vilpoux, K., Hopp, U., Harzsch, S. & Maier, G. (2005) Ontogeny of the Marmorkrebs (marbled crayfish): A parthenogenetic crayfish with unknown origin and phylogenetic position. Journal of Experimental Zoology A (Comparative and Experimental Biology), 303, 393–405.
https://doi.org/10.1002/jez.a.143Shen, H., Braband, A. & Scholtz, G. (2013) Mitogenomic analysis of decapod crustacean phylogeny corroborates traditional views on their relationships. Molecular Phylogenetics and Evolution, 66, 776–789.
https://doi.org/10.1016/j.ympev.2012.11.002
Shen, H., Braband, A. & Scholtz, G. (2015) The complete mitogenomes of lobsters and crayfish (Crustacea: Decapoda: Astacidea) reveal surprising differences in closely related taxa and convergences to Priapulida. Journal of Zoological Systematics and Evolutionary Research, 53, 273–281.
https://doi.org/10.1111/jzs.12106Sintoni, S., Benton, J.L., Beltz, B.S., Hansson, B.S. & Harzsch, S. (2012) Neurogenesis in the central olfactory pathway of adult decapod crustaceans: Development of the neurogenic niche in the brains of procambarid crayfish. Neural Development, 7, 1.
https://doi.org/10.1186/1749-8104-7-1
Soedarini, B., Klaver, L., Roessink, I., Widianarko, B., van Straalen, N.M. & van Gestel, C.A.M. (2012) Copper kinetics and internal distribution in the marbled crayfish (Procambarus sp.). Chemosphere, 87, 333–338.
https://doi.org/10.1016/j.chemosphere.2011.12.017
Soedarini, B., Klaver, L., Giesen, D., Roessink, I., Widianarko, B., van Straalen, N.M. & van Gestel, C.A.M. (2013) Effect of copper exposure on histamine concentrations in the marbled crayfish (Procambarus fallax forma virginalis). Animal Biology, 63, 139–147.
https://doi.org/10.1163/15707563-00002401Soedarini, B., van Gestel, C.A.M., van Straalen, N.M., Widianarko, B. & Röling, W.F.M. (2014) Interactions between accumulated copper, bacterial community structure and histamine levels in crayfish meat during storage. Journal of the Science of Food and Agriculture, 94, 2023–2029.
https://doi.org/10.1002/jsfa.6519Tolley, L. (2002) The Marbled Crayfish: A Study of Reproduction, Maternal Care Adaptations and Development. Bachelor's thesis. University of Manchester, Manchester, 50 pp.
Tolley, L. & Vogt, G. (2002) Reproduction of the marble crayfish, a presumptive parthenogenic decapod. 8th Colloquium Crustacea Decapoda Mediterranea, Corfu, Greece, September 2-6, 2002. Abstracts, p. 97.
Usio, N., Azuma, N., Sasaki, S., Oka, T. & Inoue, M. (2017) New record of Marmorkrebs from western Japan and its potential threats to freshwater ecosystems. Cancer, 26, 5–11. [In Japanese with English abstract]
Van Oosterhout, F., Goitom, E., Roessink, I. & Lürling, M. (2014) Lanthanum from a modified clay used in eutrophication control is bioavailable to the marbled crayfish (Procambarus fallax f. virginalis). PLoS ONE, 9, e102410.
https://doi.org/10.1371/journal.pone.0102410
Veselý, L., Buřič, M. & Kouba, A. (2015) Hardy exotics species in temperate zone: Can “warm water” crayfish invaders establish regardless of low temperatures? Scientific Reports, 5, 16340.
https://doi.org/10.1038/ srep16340Veselý, L., Hrbek, V., Kozák, P., Buřič, M., Sousa, R. & Kouba, A. (2017a) Salinity tolerance of marbled crayfish Procambarus fallax f. virginalis. Knowledge and Management of Aquatic Ecosystems, 418, 21.
https://doi.org/10.1051/kmae/2017014Veselý, L., Boukal, D.S., Buřič, M., Kozák, P., Kouba, A. & Sentis, A. (2017b) Effects of prey density, temperature and predator diversity on nonconsumptive predator-driven mortality in a freshwater food web. Scientific Reports, 7, 18075. https://doi.org/10.1038/s41598-017-17998-4
Vogt, G. (2008) The marbled crayfish: A new model organism for research on development, epigenetics and evolutionary biology. Journal of Zoology, 276, 1–13.
https://doi.org/10.1111/j.1469-7998.2008.00473.xVogt, G. (2016) Research on stem cells, aging, cancer resistance, and epigenetics in marbled crayfish and relatives: Potential benefits for human biology and medicine. In: Kawai, T., Faulkes, Z. & Scholtz, G. (Eds.), Freshwater Crayfish: A Global Overview. CRC Press, Boca Raton, pp. 115–157.
Vogt, G. (2018) Investigating the genetic and epigenetic basis of big biological questions with the parthenogenetic marbled crayfish: A review and perspective. Journal of Biosciences, 43, 189–223.
https://doi.org/10.1007/s12038-018-9741-xVogt, G. & Tolley, L. (2004) Brood care in freshwater crayfish and relationship with the offspring's sensory deficiencies. Journal of Morphology, 262, 566–582.
https://doi.org/10.1002/jmor.10169Vogt, G., Tolley, L. & Scholtz, G. (2004) Life stages and reproductive components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. Journal of Morphology, 261, 286–311.
https://doi.org/10.1002/jmor.10250Vogt, G., Huber, M., Thiemann, M., van den Boogaart, G., Schmitz, O.J. & Schubart, C.D. (2008) Production of different phenotypes from the same genotype in the same environment by developmental variation. The Journal of Experimental Biology, 211, 510–523.
https://doi.org/10.1242/jeb.008755Vogt, G., Falckenhayn, C., Schrimpf, A., Schmid, K., Hanna, K., Panteleit, J., Helm, M., Schulz, R. & Lyko, F. (2015) The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals. Biology Open, 4, 1583–1594.
https://doi.org/10.1242/bio.014241Werner, U. (1998) Garnelen, Krebse und Krabben im Süßwasseraquarium. Aqualog Verlag, Möhrfelden-Walldorf, 48 pp.