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Biologia

, Volume 73, Issue 9, pp 841–855 | Cite as

Clonal crayfish as biological model: a review on marbled crayfish

  • Md Shakhawate Hossain
  • Jiří Patoka
  • Antonín Kouba
  • Miloš Buřič
Review

Abstract

Since the mid-twentieth century, numerous vertebrates and invertebrates have been used as model organisms and become indispensable tools for exploring a broad range of biological and ecological processes. Crayfish seem to be adequate models which resulted in their involvement in research. In the two decades since its discovery, ongoing research has confirmed that the marbled crayfish (Procambarus virginalis Lyko, 2017) is an ideal taxon in this regard, especially due to its almost continuous asexual reproduction providing a source of genetically identical offspring. This review provides an overview of the occurrence, biology, ecology, ethology, and human exploitation of marbled crayfish with primary focus on its use as a laboratory model organism as well as potential risks to native biota in case of its introduction. Genetic uniformity, ease of culture, and a broad behaviour repertoire fosters the use of marbled crayfish in epigenetics and developmental biology, as well as physiological, ecotoxicological, and ethological research. Marbled crayfish could be further exploited for basic and applied fields of science such as evolutionary biology and clonal tumour evolution. However, due to its high invasive potential in freshwater environments security measures must be taken to prevent its escape into the wild.

Keywords

Model species Epigenetics Developmental biology Procambarus virginalis Biological invasion 

Notes

Acknowledgments

The study was financially supported by the Czech Science Foundation (project No. 18-03712S), Ministry of Education, Youth and Sports of the Czech Republic - projects CENAKVA (No. CZ.1.05/2.1.00/01.0024), CENAKVA II (No. LO1205 under the NPU I program), Grant Agency of University of South Bohemia (No. 017/2016/Z), and by the Internal Grant Agency of the Czech University of Life Sciences Prague (CIGA), project No. 20182013. We also deeply appreciate the assistance of the Lucidus Consultancy for the language editing of this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Abrahamsson SA (1971) Density, growth and reproduction in populations of Astacus astacus and Pacifastacus leniusculus in an isolated pond. Oikos 22:373–380.  https://doi.org/10.2307/3543861 Google Scholar
  2. Alcorlo P, Geiger W, Otero M (2008) Reproductive biology and life cycle of the invasive crayfish Procambarus clarkii (Crustacea: Decapoda) in diverse aquatic habitats of South-Western Spain: implications for population control. Fundam Appl Limnol 173:197–212.  https://doi.org/10.1127/1863-9135/2008/0173-0197 Google Scholar
  3. Alfaro J, Zúñiga G, Komen J (2004) Induction of ovarian maturation and spawning by combined treatment of serotonin and a dopamine antagonist, spiperone in Litopenaeus stylirostris and Litopenaeus vannamei. Aquaculture 236:511–522.  https://doi.org/10.1016/j.aquaculture.2003.09.020 Google Scholar
  4. Alwes F, Scholtz G (2006) Stages and other aspects of the embryology of the parthenogenetic Marmorkrebs (Decapoda, Reptantia, Astacida). Dev Genes Evol 216:169–184.  https://doi.org/10.1007/s00427-005-0041-8 Google Scholar
  5. Ameyaw-Akumfi CE (1976) Some aspects of breeding biology of crayfish. University of Michigan, DissertationGoogle Scholar
  6. Aquiloni L, Gherardi F (2008) Extended mother–offspring relationships in crayfish: the return behaviour of juvenile Procambarus clarkii. Ethology 114:946–954.  https://doi.org/10.1111/j.1439-0310.2008.01547.x Google Scholar
  7. Ashburner M, Thompson J Jr (1976) Laboratory culture of Drosophila. In: Ashburner M, Wright T (eds) The genetics and biology of Drosophila. Academic Press, pp 1–81Google Scholar
  8. Banha F, Anastácio PM (2014) Desiccation survival capacities of two invasive crayfish species. Knowl Manag Aquat Ecosyst 413:05.  https://doi.org/10.1051/kmae/2013084 Google Scholar
  9. Becking K, Haarman BCM, Riemersma van der Lek RF, Grosse L, Nolen WA, Claes S, Drexhage HA, Schoevers RA (2015) Inflammatory monocyte gene expression: trait or state marker in bipolar disorder? Int J. Bipolar Disord 3:20.  https://doi.org/10.1186/s40345-015-0037-x Google Scholar
  10. Bierbower SM (2010) Environmental effects on behavior and physiology in crayfish. Dissertation, University of KentuckyGoogle Scholar
  11. Blake M, Hart P (1993) The behavioural responses of juvenile signal crayfish Pacifastacus leniusculus to stimuli from perch and eels. Freshw Biol 29:89–97.  https://doi.org/10.1111/j.1365-2427.1993.tb00747.x Google Scholar
  12. Bohman P, Edsman L, Martin P, Scholtz G (2013) The first Marmorkrebs (Decapoda: Astacida: Cambaridae) in Scandinavia. BioInvasions Rec 2:227–232.  https://doi.org/10.3391/bir.2013.2.3.09 Google Scholar
  13. Bomirski A, Arendarczyk M, Kawinska E, Kleinholz L (1981) Partial characterization of crustacean gonad-inhibiting hormone. Int J Invertebr Reprod 3:213–219.  https://doi.org/10.1080/01651269.1981.10553396 Google Scholar
  14. Boxall AB, Rudd MA, Brooks BW, Caldwell DJ, Choi K, Hickmann S, Innes E, Ostapyk K, Staveley JP, Verslycke T (2012) Pharmaceuticals and personal care products in the environment: what are the big questions? Environ Health Perspect 120:1221–1229.  https://doi.org/10.1289/ehp.1104477 Google Scholar
  15. Brannelly LA, McMahon TA, Hinton M, Lenger D, Richards-Zawacki CL (2015) Batrachochytrium dendrobatidis in natural and farmed Louisiana crayfish populations: prevalence and implications. Dis Aquat Org 112:229–235.  https://doi.org/10.3354/dao02817 Google Scholar
  16. Bravo MA, Duarte CM, Montes C (1994) Environmental factors controlling the life history of Procambarus clarkii (Decapoda, Cambaridae) in a temporary marsh of the Doñana National Park (SW Spain). Internationale Vereinigung für Theoretische und Angewandte Limnologie, Verhandlungen 25:2450–2453Google Scholar
  17. Breithaupt T, Thiel M (2011) Chemical communication in crustaceans. Springer, New York.  https://doi.org/10.1007/978-0-387-77101-4 Google Scholar
  18. Brodin T, Fick J, Jonsson M, Klaminder J (2013) Dilute concentrations of a psychiatric drug alter behavior of fish from natural populations. Science 339:814–815.  https://doi.org/10.1126/science.1226850 Google Scholar
  19. Brodin T, Piovano S, Fick J, Klaminder J, Heynen M, Jonsson M (2014) Ecological effects of pharmaceuticals in aquatic systems-impacts through behavioural alterations. Philos Trans R Soc B Biol Sci 369:20130580.  https://doi.org/10.1098/rstb.2013.0580 Google Scholar
  20. Buřič M, Grabicová K, Kubec J, Kouba A, Kuklina I, Kozák P, Grabic R, Randák T (2018) Environmentally relevant concentrations of tramadol and citalopram alter behaviour of an aquatic invertebrate. Aquat Toxicol 200:226–232.  https://doi.org/10.1016/j.aquatox.2018.05.008
  21. Buřič M, Hulák M, Kouba A, Petrusek A, Kozák P (2011) A successful crayfish invader is capable of facultative parthenogenesis: a novel reproductive mode in decapod crustaceans. PLoS One 6:e20281.  https://doi.org/10.1371/journal.pone.0020281
  22. Buřič M, Kouba A, Kozák P (2010) Intra-sex dimorphism in crayfish females. Zoology 113:301–307.  https://doi.org/10.1016/j.zool.2010.06.001
  23. Buřič M, Kouba A, Kozák P (2013) Reproductive plasticity in freshwater invader: from long-term sperm storage to parthenogenesis. PLoS One 8:e77597.  https://doi.org/10.1371/journal.pone.0077597 Google Scholar
  24. Buřič M, Kozák P, Kouba A (2009) Movement patterns and ranging behavior of the invasive spiny-cheek crayfish in a small reservoir tributary. Fundam Appl Limnol 174:329–337.  https://doi.org/10.1127/1863-9135/2009/0174-0329 Google Scholar
  25. Capurro M, Galli L, Mori M, Salvidio S, Arillo A (2015) Reproductive cycle of Pacifastacus leniusculus (Dana) (Crustacea: Decapoda) from the Brugneto lake (Liguria, Northwest Italy). Ital J Zool 82:366–377.  https://doi.org/10.1080/11250003.2015.1022235 Google Scholar
  26. Carmona-Osalde C, Rodriguez-Serna M, Olvera-Novoa MA, Gutierrez-Yurrita PJ (2004) Gonadal development, spawning, growth and survival of the crayfish Procambarus llamasi at three different water temperatures. Aquaculture 232:305–316.  https://doi.org/10.1016/S0044-8486(03)00527-1 Google Scholar
  27. Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40.  https://doi.org/10.1111/j.1472-4642.2008.00521.x Google Scholar
  28. Cerenius L, Bangyeekhun E, Keyser P, Söderhäll I, Söderhäll K (2003) Host prophenoloxidase expression in freshwater crayfish is linked to increased resistance to the crayfish plague fungus, Aphanomyces astaci. Cell Microbiol 5:353–357.  https://doi.org/10.1046/j.1462-5822.2003.00282.x Google Scholar
  29. Chibucos K, Wofford SJ, Moore PA (2015) Hierarchical decision making: resource distribution exhibits stronger effect on crayfish dominance relationships and shelter occupation than prior social experience and resource ownership. Behaviour 152:1063–1082.  https://doi.org/10.1163/1568539X-00003292 Google Scholar
  30. Chucholl C (2011) Population ecology of an alien “warm water” crayfish (Procambarus clarkii) in a new cold habitat. Knowl Manag Aquat Ecosyst 401:1–21.  https://doi.org/10.1051/kmae/2011053 Google Scholar
  31. Chucholl C (2013) Invaders for sale: trade and determinants of introduction of ornamental freshwater crayfish. Biol Invasions 15:125–141.  https://doi.org/10.1007/s10530-012-0273-2 Google Scholar
  32. Chucholl C (2014) Predicting the risk of introduction and establishment of an exotic aquarium animal in Europe: insights from one decade of Marmorkrebs (Crustacea, Astacida, Cambaridae) releases. Manag Biol Invasion 5:309–318.  https://doi.org/10.3391/mbi.2014.5.4.01 Google Scholar
  33. Chucholl C, Morawetz K, Groß H (2012) The clones are coming–strong increase in Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] records from Europe. Aquat Invasions 7:511–519.  https://doi.org/10.3391/ai.2012.7.4.008 Google Scholar
  34. 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). Aquat Invasions 5:405–412.  https://doi.org/10.3391/ai.2010.5.4.10 Google Scholar
  35. Chucholl C, Wendler F (2017) Positive selection of beautiful invaders: long-term persistence and bio-invasion risk of freshwater crayfish in the pet trade. Biol Invasions 19:197–208.  https://doi.org/10.1007/s10530-016-1272-5 Google Scholar
  36. Chung JS, Maurer L, Bratcher M, Pitula JS, Ogburn MB (2012) Cloning of aquaporin-1 of the blue crab, Callinectes sapidus: its expression during the larval development in hyposalinity. Aquat Biosyst 8:21.  https://doi.org/10.1186/2046-9063-8-21 Google Scholar
  37. Císař P, Saberioon M, Kozák P, Pautsina A (2018) Fully contactless system for crayfish heartbeat monitoring: undisturbed crayfish as bio-indicator. Sensors Actuator B Chem 255:29–34.  https://doi.org/10.1016/j.snb.2017.07.160 Google Scholar
  38. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846.  https://doi.org/10.1038/nrg1711 Google Scholar
  39. Correia AM, Ferreira Ó (1995) Burrowing behavior of the introduced red swamp crayfish Procambarus clarkii (Decapoda: Cambaridae) in Portugal. J Crustac Biol 15:248–257.  https://doi.org/10.2307/1548953 Google Scholar
  40. Cruz MJ, Rebelo R (2007) Colonization of freshwater habitats by an introduced crayfish, Procambarus clarkii, in southwest Iberian peninsula. Hydrobiologia 575:191–201.  https://doi.org/10.1007/s10750-006-0376-9 Google Scholar
  41. Cvitanić M (2017) Reproduktivni ciklus invazivnog mramornog raka Procambarus fallax (Hagen, 1870) f. virginalis u jezeru Šoderica. University of Zagreb. Faculty of Science. Department of BiologyGoogle Scholar
  42. Delgado-Morales G, Hernandez-Falcon J, Ramon F (2004) Agonistic behaviour in crayfish: the importance of sensory inputs. Crustaceana 77:1–24.  https://doi.org/10.1163/156854004323037865 Google Scholar
  43. Dieguez-Uribeondo J, Cerenius L, Dyková I, Gelder SR, Henttonen P, Jiravanichpaisal P, Lom J, Söderhäll K (2006) Pathogens, parasites and ectocommensals. In: Souty-Grosset C, Holdich DM, Noël PY (eds) Atlas of crayfish in Europe. Museum National d’Histoire Naturelle, Paris, pp 133–149Google Scholar
  44. Diéguez-Uribeondo J, Huang T-S, Cerenius L, Söderhäll K (1995) Physiological adaptation of an Aphanomyces astaci strain isolated from the freshwater crayfish Procambarus clarkii. Mycol Res 99:574–578.  https://doi.org/10.1016/S0953-7562(09)80716-8 Google Scholar
  45. Eastman-Reks SB, Fingerman M (1985) In vitro synthesis of vitellin by the ovary of the fiddler crab, Uca pugilator. J Exp Zool 233:111–116.  https://doi.org/10.1002/jez.1402330115 Google Scholar
  46. Edgerton VR, Tillakaratne NJ, Bigbee AJ, de Leon RD, Roy RR (2004) Plasticity of the spinal neural circuitry after injury. Annu Rev Neurosci 27:145–167.  https://doi.org/10.1146/annurev.neuro.27.070203.144308 Google Scholar
  47. Espina S, Herrera FD (1993) Preferred and avoided temperatures in the crawfish Procambarus clarkii (Decapoda, Cambaridae). J Therm Biol 18:35–39.  https://doi.org/10.1016/0306-4565(93)90039-V Google Scholar
  48. Estonian Research Council (2018) Invasive marbled crayfish found in Narva power plant cooling canal. Posted at June 8, 2018 at https://phys.org/news/2018-06-invasive-marbled-crayfish-narva-power.html
  49. Fabritius-Vilpoux K, Bisch-Knaden S, Harzsch S (2008) Engrailed-like immunoreactivity in the embryonic ventral nerve cord of the marbled crayfish (Marmorkrebs). Invertebr Neurosci 8:177.  https://doi.org/10.1007/s10158-008-0081-7 Google Scholar
  50. Falckenhayn C (2017) The methylome of the marbled crayfish Procambarus virginalis. University of Heildelberg, DissertationGoogle Scholar
  51. Farca Luna AJ, Hurtado-Zavala JI, Reischig T, Heinrich R (2009) Circadian regulation of agonistic behavior in groups of parthenogenetic marbled crayfish, Procambarus sp. J Biol Rhythm 24:64–72.  https://doi.org/10.1177/0748730408328933 Google Scholar
  52. Faulkes Z (2010) The spread of the parthenogenetic marbled crayfish, Marmorkrebs (Procambarus sp.), in the north American pet trade. Aquat Invasions 5:447–450.  https://doi.org/10.3391/ai.2010.5.4.16 Google Scholar
  53. Faulkes Z (2013) How much is that crayfish in the window? Online monitoring of Marmorkrebs, Procambarus fallax f. virginalis (Hagen, 1870) in the north American pet trade. Freshw Crayfish 19:39–44Google Scholar
  54. Faulkes Z (2015) Marmorkrebs (Procambarus fallax f. virginalis) are the most popular crayfish in the north American pet trade. Knowl Manag Aquat Ecosyst 416:1–15.  https://doi.org/10.1051/kmae/2015016 Google Scholar
  55. Faulkes Z, Feria TP, Muñoz J (2012) Do Marmorkrebs, Procambarus fallax f. virginalis, threaten freshwater Japanese ecosystems? Aquat Biosyst 8:13.  https://doi.org/10.1186/2046-9063-8-13 Google Scholar
  56. Feria TP, Faulkes Z (2011) Forecasting the distribution of Marmorkrebs, a parthenogenetic crayfish with high invasive potential, in Madagascar, Europe, and North America. Aquat Invasions 6:55–67.  https://doi.org/10.3391/ai.2011.6.1.07 Google Scholar
  57. Fero KC, Moore PA (2014) Shelter availability influences social behavior and habitat choice in crayfish, Orconectes virilis. Behaviour 151:103–123.  https://doi.org/10.1163/1568539X-00003125 Google Scholar
  58. Figler MH, Blank GS, Peeke HV (1997) Maternal aggression and post-hatch care in red swamp crayfish, Procambarus clarkii (Girard): the influences of presence of offspring, fostering, and maternal molting. Mar Freshw Behav Physiol 30:173–194.  https://doi.org/10.1080/10236249709379023 Google Scholar
  59. Figler MH, Blank GS, Peeke HV (2001) Maternal territoriality as an offspring defense strategy in red swamp crayfish (Procambarus clarkii, Girard). Aggress Behav 27:391–403.  https://doi.org/10.1002/ab.1024 Google Scholar
  60. Fingerman M, Nagabhushanam R, Sarojini R, Reddy PS (1994) Biogenic amines in crustaceans: identification, localization, and roles. J Crustac Biol 14:413–437.  https://doi.org/10.2307/1548990 Google Scholar
  61. Fossat P, Bacqué-Cazenave J, De Deurwaerdère P, Delbecque J-P, Cattaert D (2014) Anxiety-like behavior in crayfish is controlled by serotonin. Science 344:1293–1297.  https://doi.org/10.1126/science.1248811 Google Scholar
  62. Fossat P, Bacqué-Cazenave J, De Deurwaerdère P, Cattaert D, Delbecque J-P (2015) Serotonin, but not dopamine, controls the stress response and anxiety-like behavior in the crayfish Procambarus clarkii. J Exp Biol 218:2745–2752.  https://doi.org/10.1242/jeb.120550 Google Scholar
  63. Gherardi F (2002) Behaviour. In: Holdich DM (ed) Biology of freshwater crayfish. Blackwell Science, Oxford, pp 258–290. https://doi.org/10.1651/0278-0372(2002)022[0969:BOFC]2.0.CO;2Google Scholar
  64. Gherardi F, Souty-Grosset C, Vogt G, Diéguez-Uribeondo J, Crandall KA (2010) Infraorder Astacidea Latreille, 1802. In: The freshwater crayfish. Treatise on Zoology, Anatomy, Taxonomy, Biology The Crustacea, Decapoda. Brill, Leiden, pp 269–423Google Scholar
  65. Guan R-Z, Wiles P (1997) The home range of the signal crayfish in a British lowland river. Freshw Forum 1997:45–54Google Scholar
  66. Guan R-Z, Wiles PR (1999) Growth and reproduction of the introduced crayfish Pacifastacus leniusculus in a British lowland river. Fish Res 42:245–259.  https://doi.org/10.1016/S0165-7836(99)00044-2 Google Scholar
  67. Gutekunst J, Andriantsoa R, Falckenhayn C, Hanna K, Stein W, Rasamy J, Lyko F (2018) Clonal genome evolution and rapid invasive spread of the marbled crayfish. Nat Ecol Evol 2:567–573.  https://doi.org/10.1038/s41559-018-0467-9 Google Scholar
  68. Herberholz J, McCurdy C, Edwards DH (2007) Direct benefits of social dominance in juvenile crayfish. Biol Bull 213:21–27.  https://doi.org/10.2307/25066615 Google Scholar
  69. Herberholz J, Sen MM, Edwards DH (2004) Escape behavior and escape circuit activation in juvenile crayfish during prey–predator interactions. J Exp Biol 207:1855–1863.  https://doi.org/10.1242/jeb.00992 Google Scholar
  70. Herrmann A, Schnabler A, Martens A (2018) Phenology of overland dispersal in the invasive crayfish Faxonius immunis (Hagen) at the upper Rhine River area. Knowl Manage of Aquat Ecosyst, in pressGoogle Scholar
  71. Hill AM, Lodge DM (1999) Replacement of resident crayfishes by an exotic crayfish: the roles of competition and predation. Ecol Appl 9:678–690. https://doi.org/10.1890/1051-0761(1999)009[0678:RORCBA]2.0.CO;2Google Scholar
  72. Hill RW, Wyse GA, Anderson M (2004) Animal physiology. Sinauer Associates Massachusetts, USAGoogle Scholar
  73. Holdich D (2002) Background and functional morphology. In: Holdich D (ed) Biology of freshwater crayfish. Blackwell Science Oxford, London, UK, pp 3–29. https://doi.org/10.1651/0278-0372(2002)022[0969:BOFC]2.0.CO;2Google Scholar
  74. Holdich D, Reader J, Rogers W, Harlioglu M (1995) Interactions between three species of crayfish (Austropotamobius pallipes, Astacus leptodactylus and Pacifastacus leniusculus). Freshw Crayfish 10:46–56Google Scholar
  75. Holdich DM, Haffner P, Noël P (2006) Species files. In: Souty-Grosset C, Holdich DM, Noël PY, Reynolds JD, Haffner P (eds) Atlas of crayfish in Europe. Museum National d’Histoire Naturelle, Paris, pp 50–129Google Scholar
  76. Hsieh C-Y, Huang C-W, Pan Y-C (2016) Crayfish plague Aphanomyces astaci detected in redclaw crayfish, Cherax quadricarinatus in Taiwan. J Invertebr Pathol 136:117–123.  https://doi.org/10.1016/j.jip.2016.03.015 Google Scholar
  77. Hunter P (2008) The paradox of model organisms. EMBO Rep 9:717–720.  https://doi.org/10.1038/embor.2008.142 Google Scholar
  78. Jackson CJ (2016) Characterization of locomotor response to psychostimulants in the parthenogenetic marbled crayfish (Procambarus fallax forma virginalis): a promising model for studying the epigenetics of addiction. Bowling Green State University, DissertationGoogle Scholar
  79. James J, Mrugała A, Oidtmann B, Petrusek A, Cable J (2017) Apparent interspecific transmission of Aphanomyces astaci from invasive signal to virile crayfish in a sympatric wild population. J Invertebr Pathol 145:68–71.  https://doi.org/10.1016/j.jip.2017.02.003 Google Scholar
  80. Janský V, Mutkovič A (2010) Rak Procambarus sp. (Crustacea: Decapoda: Cambaridae)–prvý nález na Slovensku. Zbornik Slovenského Národneho Múzea (Acta Rerum Naturalium Musei Nationalis Slovaci Bratislava) 56:64–67Google Scholar
  81. Jeschke JM, Strayer DL (2005) Invasion success of vertebrates in Europe and North America. Proc Natl Acad Sci U S A 102:7198–7202.  https://doi.org/10.1073/pnas.0504835102 Google Scholar
  82. Jimenez SA, Faulkes Z (2010) Establishment and care of a colony of parthenogenetic marbled crayfish, Marmorkrebs. Invertebr Rearing 1:10–18Google Scholar
  83. Jimenez SA, Faulkes Z (2011) Can the parthenogenetic marbled crayfish Marmorkrebs compete with other crayfish species in fights? J Ethol 29:115–120.  https://doi.org/10.1007/s10164-010-0232-2 Google Scholar
  84. Jirikowski G, Kreissl S, Richter S, Wolff C (2010) Muscle development in the marbled crayfish—insights from an emerging model organism (Crustacea, Malacostraca, Decapoda). Dev Genes Evol 220:89–105.  https://doi.org/10.1007/s00427-010-0331-7 Google Scholar
  85. Jones JP, Rasamy JR, Harvey A, Toon A, Oidtmann B, Randrianarison MH, Raminosoa N, Ravoahangimalala OR (2009) The perfect invader: a parthenogenic crayfish poses a new threat to Madagascar’s freshwater biodiversity. Biol Invasions 11:1475–1482.  https://doi.org/10.1007/s10530-008-9334-y Google Scholar
  86. Kaldre K, Meženin A, Paaver T, Kawai T (2016) A preliminary study on the tolerance of marble crayfish Procambarus fallax f. virginalis to low temperature in Nordic climate. In: Kawai T, Faulkes Z, Scholtz G (eds) Freshwater crayfish: a global overview. CRC Press, New York, pp 54–62Google Scholar
  87. Kawai T, Faulkes Z, Scholtz G (2016) Freshwater crayfish: a global overview. CRC Press, New YorkGoogle Scholar
  88. Kawai T, Takahata M (eds) (2010) Biology of crayfish. Hokkaido University Press, SapporoGoogle Scholar
  89. Keller N, Pfeiffer M, Roessink I, Schulz R, Schrimpf A (2014) First evidence of crayfish plague agent in populations of the marbled crayfish (Procambarus fallax forma virginalis). Knowl Manag Aquat Ecosyst 414:8.  https://doi.org/10.1051/kmae/2014032 Google Scholar
  90. Kotovska G, Khrystenko D, Patoka J, Kouba A (2016) East European crayfish stocks at risk: arrival of non-indigenous crayfish species. Knowl Manag Aquat Ecosyst 417:37.  https://doi.org/10.1051/kmae/2016024 Google Scholar
  91. Kouba A, Buřič M, Kozák P (2010) Bioaccumulation and effects of heavy metals in crayfish: a review. Water Air Soil Pollut 211:5–16.  https://doi.org/10.1007/s11270-009-0273-8 Google Scholar
  92. Kouba A, Petrusek A, Kozák P (2014) Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Manag Aquat Ecosyst 413:1–31.  https://doi.org/10.1051/kmae/2014007 Google Scholar
  93. 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. Sci Rep 6:26569.  https://doi.org/10.1038/srep26569 Google Scholar
  94. Koutnik D, Stara A, Zuskova E, Kouba A, Velisek J (2017) The chronic effects of terbuthylazine-2-hydroxy on early life stages of marbled crayfish (Procambarus fallax f. virginalis). Pestic Biochem Physiol 136:29–33.  https://doi.org/10.1016/j.pestbp.2016.08.008 Google Scholar
  95. Kozák P, Buřič M, Policar T (2006) The fecundity, time of egg development and juvenile production in spiny-cheek crayfish (Orconectes limosus) under controlled conditions. Bull Fr Pêche Piscic 380-381:1171–1182.  https://doi.org/10.1051/kmae:2006019 Google Scholar
  96. Kozák P, Ďuriš Z, Petrusek A, Buřič M, Horká I, Kouba A, Policar T (2015) Crayfish biology and culture. University of South Bohemia in Ceske Budejovice. Faculty of Fisheries and Protection of Waters, VodnanyGoogle Scholar
  97. Kozubíková E, Filipová L, Kozák P, Ďuriš Z, Martín MP, Diéguez-Uribeondo J, Oidtmann B, Petrusek A (2009) Prevalence of the crayfish plague pathogen Aphanomyces astaci in invasive American crayfishes in the Czech Republic. Conserv Biol 23:1204–1213.  https://doi.org/10.1111/j.1523-1739.2009.01240.x Google Scholar
  98. Kozubíková-Balcarová E, Beran L, Ďuriš Z, Fischer D, Horká I, Svobodová J, Petrusek A (2014) Status and recovery of indigenous crayfish populations after recent crayfish plague outbreaks in the Czech Republic. Ethol Ecol Evol 26:299–319.  https://doi.org/10.1080/03949370.2014.897652 Google Scholar
  99. Kravitz EA (2000) Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. J Comp Physiol A-Neuroethol Sens Neural Behav Physiol 186:221–238.  https://doi.org/10.1007/s003590050423 Google Scholar
  100. Kuo C-M, Chen Y-N, Fan H-F, Chuang H-C, Hsieh S-L (2009) Enhancement of vitellogenin synthesis by serotonin in the giant freshwater prawn Macrobrachium rosenbergii (De man). Zool Stud 48:597–606Google Scholar
  101. Lahman SE, Trent KR, Moore PA (2015) Sublethal copper toxicity impairs chemical orientation in the crayfish, Orconectes rusticus. Ecotoxicol Environ Saf 113:369–377.  https://doi.org/10.1016/j.ecoenv.2014.12.022 Google Scholar
  102. Larson ER, Twardochleb LA, Olden JD (2016) Comparison of trophic function between the globally invasive crayfishes Pacifastacus leniusculus and Procambarus clarkii. Limnology 18:275–286.  https://doi.org/10.1007/s10201-016-0505-8 Google Scholar
  103. Laufer H, Ahl JS, Sagi A (1993) The role of juvenile hormones in crustacean reproduction. Integr Comp Biol 33:365–365.  https://doi.org/10.1093/icb/33.3.365 Google Scholar
  104. Laxmyr L (1984) Biogenic amines and dopa in the central nervous system of decapod crustaceans. Comp Biochem Physiol C-Comp Pharmacol 7:139–143.  https://doi.org/10.1016/0742-8413(84)90142-7 Google Scholar
  105. Lidova J, Stara A, Kouba A, Velisek J (2016) The effects of cypermethrin on oxidative stress and antioxidant biomarkers in marbled crayfish (Procambarus fallax f. virginalis). Neuroendocrinol Lett 37:1Google Scholar
  106. Lipták B, Mojžišová M, Gruĺa D, Christophoryová J, Jablonski D, Bláha M, Petrusek A, Kouba A (2017) Slovak section of the Danube has its well-established breeding ground of marbled crayfish Procambarus fallax f. virginalis. Knowl Manag Aquat Ecosyst 418:1–5.  https://doi.org/10.1051/kmae/2017029 Google Scholar
  107. Lipták B, Mrugała A, Pekárik L, Mutkovič A, Gruľa D, Petrusek A, Kouba A (2016) Expansion of the marbled crayfish in Slovakia: beginning of an invasion in the Danube catchment? J Limnol 75:305–312.  https://doi.org/10.4081/jlimnol.2016.1313 Google Scholar
  108. Lipták B, Vitázková B (2015) Beautiful, but also potentially invasive. Ekológia (Bratislava) 34:155–162.  https://doi.org/10.1515/eko-2015-0016 Google Scholar
  109. Little EE (1975) Chemical communication in maternal behaviour of crayfish. Nature 255:400–401.  https://doi.org/10.1038/255400a0 Google Scholar
  110. Lőkkös A, Müller T, Kovács K, Várkonyi L, Specziár A, Martin P (2016) The alien, parthenogenetic marbled crayfish (Decapoda: Cambaridae) is entering Kis-Balaton (Hungary), one of Europe’s most important wetland biotopes. Knowl Manag Aquat Ecosyst 417:1–9.  https://doi.org/10.1051/kmae/2016003 Google Scholar
  111. Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world's worst invasive alien species: a selection from the global invasive species database. vol 12. Invasive Species Specialist Group AucklandGoogle Scholar
  112. Lukhaup C (2001) Procambarus sp.–der Marmorkrebs. Aquaristik Aktuell 7-8:48–51Google Scholar
  113. Lyko F (2017) The marbled crayfish (Decapoda: Cambaridae) represents an independent new species. Zootaxa 4363:544–552.  https://doi.org/10.11646/zootaxa.4363.4.6 Google Scholar
  114. Makkonen J, Jussila J, Kortet R, Vainikka A, Kokko H (2012) Differing virulence of Aphanomyces astaci isolates and elevated resistance of noble crayfish Astacus astacus against crayfish plague. Dis Aquat Org 102:129–136.  https://doi.org/10.3354/dao02547 Google Scholar
  115. Marenkov O, Kovalchuk J, Shapovalenko Z, Naboka O, Nesterenko O, Dzhobolda B (2017) Parameters of the histological adaptation of Marmorkrebs Procambarus fallax f. virginalis (Decapoda, Cambaridae) to zinc and cadmium ions pollution. World Sci News 90:189–202Google Scholar
  116. Marten M, Werth C, Marten D (2004) Der Marmorkrebs (Cambaridae, Decapoda) in Deutschland–ein weiteres Neozoon im Einzugsgebiet des Rheins. Lauterbornia 50:17–23Google Scholar
  117. Martin P (2015) Parthenogenesis: mechanisms, evolution, and its relevance to the role of marbled crayfish as model organism and potential invader. In: Kawai T, Faulkes, Scholtz G (eds) Freshwater crayfish: a global overview. CRC Press, New York, pp 63–82Google Scholar
  118. Martin P, Dorn NJ, Kawai T, van der Heiden C, Scholtz G (2010a) The enigmatic Marmorkrebs (marbled crayfish) is the parthenogenetic form of Procambarus fallax (Hagen, 1870). Contrib Zool 79:107–118Google Scholar
  119. 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/s00114-007-0260-0 Google Scholar
  120. Martin P, Scholtz G (2012) A case of intersexuality in the parthenogenetic Marmorkrebs (Decapoda: Astacida: Cambaridae). J Crustac Biol 32:345–350.  https://doi.org/10.1163/193724012X629031 Google Scholar
  121. Martin P, Shen H, Füllner G, Scholtz G (2010b) The first record of the parthenogenetic Marmorkrebs (Decapoda, Astacida, Cambaridae) in the wild in Saxony (Germany) raises the question of its actual threat to European freshwater ecosystems. Aquat Invasions 5:397–403.  https://doi.org/10.3391/ai.2010.5.4.09 Google Scholar
  122. Martin P, Thonagel S, Scholtz G (2016) The parthenogenetic Marmorkrebs (Malacostraca: Decapoda: Cambaridae) is a triploid organism. J Zool Syst Evol Res 54:13–21.  https://doi.org/10.1111/jzs.12114 Google Scholar
  123. Mathews LM (2011) Mother-offspring recognition and kin-preferential behaviour in the crayfish Orconectes limosus. Behaviour 148:71–87.  https://doi.org/10.1163/000579510X548600 Google Scholar
  124. Merkle EL (1969) Home range of crayfish Orconectes juvenalis. Am Midl Nat 81:228–235.  https://doi.org/10.2307/2423664 Google Scholar
  125. Mrugała A, Kozubíková-Balcarová E, Chucholl C, Resino SC, Viljamaa-Dirks S, Vukić J, Petrusek A (2015) Trade of ornamental crayfish in Europe as a possible introduction pathway for important crustacean diseases: crayfish plague and white spot syndrome. Biol Invasions 17:1313–1326.  https://doi.org/10.1007/s10530-014-0795-x Google Scholar
  126. Neal AE, Moore PA (2017) Mimicking natural systems: changes in behavior as a result of dynamic exposure to naproxen. Ecotoxicol Environ Safe 135:347–357.  https://doi.org/10.1016/j.ecoenv.2016.10.015 Google Scholar
  127. Nonnis-Marzano F, Scalici M, Chiesa S, Gherardi F, Piccinini A, Gibertini G (2009) The first record of the marbled crayfish adds further threats to fresh waters in Italy. Aquat Invasions 4:401–404.  https://doi.org/10.3391/ai.2009.4.2.19 Google Scholar
  128. Novitsky RA, Son MO (2016) The first records of Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] (Crustacea, Decapoda, Cambaridae) in Ukraine. Ecologica Montenegrina 5:44–46Google Scholar
  129. Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437.  https://doi.org/10.1146/annurev.genet.34.1.401 Google Scholar
  130. Pârvulescu L, Togor A, Lele S-F, Scheu S, Șinca D, Panteleit J (2017) First established population of marbled crayfish Procambarus fallax (Hagen, 1870) f. virginalis (Decapoda, Cambaridae) in Romania. BioInvasions Rec 6:357–362.  https://doi.org/10.3391/bir.2017.6.4.09 Google Scholar
  131. Patoka J, Bláha M, Kalous L, Kouba A (2016a) Irresponsible vendors: non-native, invasive and threatened animals offered for garden pond stocking. Aquat Conserv Mar Freshwat Ecosyst 27:692–697.  https://doi.org/10.1002/aqc.2719 Google Scholar
  132. Patoka J, Buřič M, Kolář V, Bláha M, Petrtýl M, Franta P, Tropek R, Kalous L, Petrusek A, Kouba A (2016b) Predictions of marbled crayfish establishment in conurbations fulfilled: evidences from the Czech Republic. Biologia 71:1380–1385.  https://doi.org/10.1515/biolog-2016-0164 Google Scholar
  133. Patoka J, Petrtýl M, Kalous L (2014) Garden ponds as potential introduction pathway of ornamental crayfish. Knowl Manag Aquat Ecosyst 414:1–8.  https://doi.org/10.1051/kmae/2014019 Google Scholar
  134. Patoka J, Petrtýl M, Kosčo J, Rylkova K (2015) Juvenile red swamp crayfish growth affected by isolation from their mother. Biologia 70:632–635.  https://doi.org/10.1515/biolog-2015-0069 Google Scholar
  135. Payette AL, McGaw IJ (2003) Thermoregulatory behavior of the crayfish Procambarus clarkii in a burrow environment. Comp Biochem Physiol A Mol Integr Physiol 136:539–556.  https://doi.org/10.1016/S1095-6433(03)00203-4 Google Scholar
  136. Peay S (2009) Invasive non-indigenous crayfish species in Europe: recommendations on managing them. Knowl Manag Aquat Ecosyst 394-395:03.  https://doi.org/10.1051/kmae/2010009 Google Scholar
  137. Peay S, Holdich D, Brickland J (2010) Risk assessments of non-indigenous crayfish in Great Britain. Freshw Crayfish 17:109–122Google Scholar
  138. Pfeiffer M (2005) Marmorkrebse überleben im eis. Fischer Teichwirt 6:204Google Scholar
  139. Puky M (2014) Invasive crayfish on land: Orconectes limosus (Rafinesque, 1817)(Decapoda: Cambaridae) crossed a terrestrial barrier to move from a side arm into the Danube river at Szeremle, Hungary. Acta Zool Bulg 7:143–146Google Scholar
  140. Quackenbush LS (1989) Vitellogenesis in the shrimp, Penaeus vannamei: in vitro studies of the isolated hepatopancreas and ovary. Comp Biochem Physiol B Comp Biochem 94:253–261.  https://doi.org/10.1016/0305-0491(89)90342-8 Google Scholar
  141. Ramalho RMO (2012) Dispersal and population regulation of the red swamp crayfish (Procambarus clarkii). University of Evora, DissertationGoogle Scholar
  142. Resetarits WJ (1991) Ecological interactions among predators in experimental stream communities. Ecology 72:1782–1793.  https://doi.org/10.2307/1940977 Google Scholar
  143. Reynolds J (2002) Growth and reproduction. In: Holdich DM (ed) Biology of freshwater crayfish. Blackwell Science, Oxford, pp 152–191. https://doi.org/10.1651/0278-0372(2002)022[0969:BOFC]2.0.CO;2Google Scholar
  144. Reynolds J, Demers A, Marnell F (2002) Managing an abundant crayfish resource for conservation A. pallipes in Ireland. Bull Fr Pêche Piscic 367:823–832.  https://doi.org/10.1051/kmae:2002070 Google Scholar
  145. Reynolds J, Souty-Grosset C, Richardson A, Reynolds J (2012) Crayfish as prime players in ecosystems: life-history strategies. In: Reynolds J (ed) Management of freshwater biodiversity. Crayfish as bioindicators. Cambridge University Press, Cambridge, pp 59–82Google Scholar
  146. Rezinciuc S, Galindo J, Montserrat J, Diéguez-Uribeondo J (2014) AFLP-PCR and RAPD-PCR evidences of the transmission of the pathogen Aphanomyces astaci (oomycetes) to wild populations of European crayfish from the invasive crayfish species, Procambarus clarkii. Fungal Biol 118:612–620.  https://doi.org/10.1016/j.funbio.2013.10.007 Google Scholar
  147. Rhodes C, Holdich D (1979) On size and sexual dimorphism in Austropotamobius pallipes (Lereboullet): a step in assessing the commercial exploitation potential of the native British freshwater crayfish. Aquaculture 17:345–358.  https://doi.org/10.1016/0044-8486(79)90089-9 Google Scholar
  148. Rieger V, Harzsch S (2008) Embryonic development of the histaminergic system in the ventral nerve cord of the marbled crayfish (Marmorkrebs). Tissue Cell 40:113–126.  https://doi.org/10.1016/j.tice.2007.10.004 Google Scholar
  149. Samardžić M, Lucić A, Maguire I, Hudina S (2014) The first record of the marbled crayfish (Procambarus fallax (Hagen, 1870) f. virginalis) in Croatia. Crayfish News 36:4–4Google Scholar
  150. Schneider RAZ, Schneider RWS, Moore PA (1999) Recognition of dominance status by chemoreception in the red swamp crayfish, Procambarus clarkii. J Chem Ecol 25:781–794.  https://doi.org/10.1023/A:1020888532513 Google Scholar
  151. Scholtz G (2015) 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 3–12Google Scholar
  152. Scholtz G, Braband A, Tolley L, Reimann A, Mittman B, Lukhaup C, Steuerwald F, Vogt G (2003) Ecology: parthenogenesis in an outsider crayfish. Nature 421:806.  https://doi.org/10.1038/421806a Google Scholar
  153. Seitz R (2001) Lebensdaten und Reproduktionsbiologie des Marmorkrebses (Crustacea: Decapoda). University Ulm, DissertationGoogle Scholar
  154. 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. J Exp Zool A Ecol Genet Physiol 303:393–405.  https://doi.org/10.1002/jez.a.143 Google Scholar
  155. Shave CR, Townsend CR, Crowl TA (1994) Anti-predator behaviours of a freshwater crayfish (Paranephrops zealandicus) to a native and an introduced predator. N Z J Ecol 18:1–10Google Scholar
  156. Simon J-C, Delmotte F, Rispe C, Crease T (2011) Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biol J Linn Soc 79:151–163.  https://doi.org/10.1046/j.1095-8312.2003.00175.x Google Scholar
  157. Singer E (2016) Biologists search for new model organisms: the bulk of biological research is centered on a handful of species. Are we missing a huge chunk of life's secrets? https://www.quantamagazine.org/20160726-model-organisms/. Accessed 19 march, 2018
  158. Singleman C, Holtzman NG (2014) Growth and maturation in the zebrafish, Danio rerio: a staging tool for teaching and research. Zebrafish 11:396–406.  https://doi.org/10.1089/zeb.2014.0976 Google Scholar
  159. Sintoni S, Fabritius-Vilpoux K, Harzsch S (2007) The engrailed-expressing secondary head spots in the embryonic crayfish brain: examples for a group of homologous neurons in Crustacea and Hexapoda? Dev Genes Evol 217:791–799.  https://doi.org/10.1007/s00427-007-0189-5 Google Scholar
  160. Sneddon LU, Taylor AC, Huntingford FA, Watson DG (2000) Agonistic behaviour and biogenic amines in shore crabs Carcinus maenas. J Exp Biol 203:537–545Google Scholar
  161. Soes M, Koese B (2010) Invasive freshwater crayfish in the Netherlands: a preliminary risk analysis. Stichting Eis-Nederland, Leiden & Bureau Waardenburg, CulemborgGoogle Scholar
  162. Souty-Grosset C, Anastácio PM, Aquiloni L, Banha F, Choquer J, Chucholl C, Tricarico E (2016) The red swamp crayfish Procambarus clarkii in Europe: impacts on aquatic ecosystems and human well-being. Limnol-Ecol Manage Inland Waters 58:78–93.  https://doi.org/10.1016/j.limno.2016.03.003 Google Scholar
  163. Souty-Grosset C, Holdich DM, Noël PY (2006) Atlas of crayfish in Europe. Collection Patrimoines Naturels. Muséum National d'Histoire Naturelle, ParisGoogle Scholar
  164. Stebbing P (2016) The management of invasive crayfish. In: Biology and ecology of crayfish. CRC Press, Boca Raton, pp 337–357Google Scholar
  165. Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca RatonGoogle Scholar
  166. Svoboda J, Mrugała A, Kozubíková-Balcarová E, Petrusek A (2017) Hosts and transmission of the crayfish plague pathogen Aphanomyces astaci: a review. J Fish Dis 40:127–140.  https://doi.org/10.1111/jfd.12472 Google Scholar
  167. Takahashi K, Nagayama T (2016) Shelter preference in the Marmorkrebs (marbled crayfish). Behaviour 153:1913–1930.  https://doi.org/10.1163/1568539X-00003399 Google Scholar
  168. Takayanagi H, Yamamoto Y, Takeda N (1986) An ovary-stimulating factor in the shrimp, Paratya compressa. J Exp Zool A Ecol Genet Physiol 240:203–209.  https://doi.org/10.1002/jez.1402400208 Google Scholar
  169. Taylor CA, Warren ML Jr, Fitzpatrick J Jr, Hobbs HH III, Jezerinac RF, Pflieger WL, Robison HW (1996) Conservation status of crayfishes of the United States and Canada. Fisheries 21:25–38.  https://doi.org/10.1577/1548-8446(1996)021<0025:CSOCOT>2.0.CO;2 Google Scholar
  170. Thiel M (2007) Social behaviour of parent–offspring groups in crustaceans. In: Duffy JE, Thiel M (eds) Evolutionary ecology of social and sexual systems: crustaceans as model organisms. Oxford University Press, Oxford, pp 294–318Google Scholar
  171. Uderbayev T, Patoka J, Beisembayev R, Petrtýl M, Bláha M, Kouba A (2017) Risk assessment of pet-traded decapod crustaceans in the Republic of Kazakhstan, the leading country in Central Asia. Knowl Manag Aquat Ecosyst 418:30.  https://doi.org/10.1051/kmae/2017018 Google Scholar
  172. Unestam T (1972) On the host range and origin of the crayfish plague fungus. Rep Inst Freshw Res Drottningholm 52:192–198Google Scholar
  173. 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 26:5–11Google Scholar
  174. Vaca AA, Alfaro J (2000) Ovarian maturation and spawning in the white shrimp, Penaeus vannamei, by serotonin injection. Aquaculture 182:373–385.  https://doi.org/10.1016/S0044-8486(99)00267-7 Google Scholar
  175. Valenti TW Jr, Gould GG, Berninger JP, Connors KA, Keele NB, Prosser KN, Brooks BW (2012) Human therapeutic plasma levels of the selective serotonin reuptake inhibitor (ssri) sertraline decrease serotonin reuptake transporter binding and shelter-seeking behavior in adult male fathead minnows. Environ Sci Technol 46:2427–2435.  https://doi.org/10.1021/es204164b Google Scholar
  176. Velíšek J, Stará A, Zusková E, Kubec J, Buřič M, Kouba A (2018) Chronic toxicity of metolachlor OA on growth, ontogenetic development, antioxidant biomarkers and histopathology of early life stages of marbled crayfish. Sci Total Environ 643:1456–1463.  https://doi.org/10.1016/j.scitotenv.2018.06.309 Google Scholar
  177. Veselý L, Boukal DS, Buřič M, Kozák P, Kouba A, Sentis A (2017) Effects of prey density, temperature and predator diversity on nonconsumptive predator-driven mortality in a freshwater food web. Sci Rep 7:18075.  https://doi.org/10.1038/s41598-017-17998-4 Google Scholar
  178. Veselý L, Buřič M, Kouba A (2015) Hardy exotics species in temperate zone: can “warm water” crayfish invaders establish regardless of low temperatures? Sci Rep 5:16340.  https://doi.org/10.1038/srep16340 Google Scholar
  179. Viljamaa-Dirks S, Heinikainen S, Torssonen H, Pursiainen M, Mattila J, Pelkonen S (2013) Distribution and epidemiology of genotypes of the crayfish plague agent Aphanomyces astaci from noble crayfish Astacus astacus in Finland. Dis Aquat Org 103:199–208.  https://doi.org/10.3354/dao02575 Google Scholar
  180. Vilpoux K, Sandeman R, Harzsch S (2006) Early embryonic development of the central nervous system in the Australian crayfish and the marbled crayfish (Marmorkrebs). Dev Genes Evol 216:209–223.  https://doi.org/10.1007/s00427-005-0055-2 Google Scholar
  181. Vodovsky N, Patoka J, Kouba A (2017) Ecosystem of Caspian Sea threatened by pet-traded non-indigenous crayfish. Biol Invasions 19:2207–2217.  https://doi.org/10.1007/s10530-017-1433-1 Google Scholar
  182. Vogt G (2002) Functional anatomy. In: Holdich DM (ed) Biology of freshwater crayfish. Blackwell Science, Oxford, pp 53–151. https://doi.org/10.1651/0278-0372(2002)022[0969:BOFC]2.0.CO;2Google Scholar
  183. Vogt G (2007) Exposure of the eggs to 17alpha-methyl testosterone reduced hatching success and growth and elicited teratogenic effects in postembryonic life stages of crayfish. Aquat Toxicol 85:291–296.  https://doi.org/10.1016/j.aquatox.2007.09.012 Google Scholar
  184. Vogt G (2008a) How to minimize formation and growth of tumours: potential benefits of decapod crustaceans for cancer research. Int J Cancer 123:2727–2734.  https://doi.org/10.1002/ijc.23947 Google Scholar
  185. Vogt G (2008b) Investigation of hatching and early post-embryonic life of freshwater crayfish by in vitro culture, behavioral analysis, and light and electron microscopy. J Morphol 269:790–811.  https://doi.org/10.1002/jmor.10622 Google Scholar
  186. Vogt G (2008c) The marbled crayfish: a new model organism for research on development, epigenetics and evolutionary biology. J Zool 276:1–13.  https://doi.org/10.1111/j.1469-7998.2008.00473.x Google Scholar
  187. Vogt G (2010) Suitability of the clonal marbled crayfish for biogerontological research: a review and perspective, with remarks on some further crustaceans. Biogerontology 11:643–669.  https://doi.org/10.1007/s10522-010-9291-6 Google Scholar
  188. Vogt G (2011) Marmorkrebs: natural crayfish clone as emerging model for various biological disciplines. J Biosci 36:377–382.  https://doi.org/10.1007/s12038-011-9070-9 Google Scholar
  189. Vogt G (2012) Ageing and longevity in the Decapoda (Crustacea): a review. Zool Anz 251:1–25.  https://doi.org/10.1016/j.jcz.2011.05.003 Google Scholar
  190. Vogt G (2013) Abbreviation of larval development and extension of brood care as key features of the evolution of freshwater Decapoda. Biol Rev 88:81–116.  https://doi.org/10.1111/j.1469-185X.2012.00241.x Google Scholar
  191. Vogt G (2015) Bimodal annual reproductive pattern in laboratory-reared marbled crayfish. Invertebr Reprod Dev 59:218–223.  https://doi.org/10.1080/07924259.2015.1089329 Google Scholar
  192. Vogt G (2017) Facilitation of environmental adaptation and evolution by epigenetic phenotype variation: insights from clonal, invasive, polyploid, and domesticated animals. Environ Epigenet 3:dvx002.  https://doi.org/10.1093/eep/dvx002 Google Scholar
  193. Vogt G (2018b) Annotated bibliography of the parthenogenetic marbled crayfish, Procambarus virginalis, a new research model, potent invader and popular pet. Zootaxa 4418:301–352.  https://doi.org/10.11646/zootaxa.4418.4.1 Google Scholar
  194. Vogt 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. Biol Open 4:1583–1594.  https://doi.org/10.1242/bio.014241 Google Scholar
  195. Vogt G, Huber M, Thiemann M, van den Boogaart G, Schmitz OJ, Schubart CD (2008) Production of different phenotypes from the same genotype in the same environment by developmental variation. J Exp Biol 211:510–523.  https://doi.org/10.1242/jeb.008755 Google Scholar
  196. Vogt G, Tolley L (2004) Brood care in freshwater crayfish and relationship with the offspring's sensory deficiencies. J Morphol 262:566–582.  https://doi.org/10.1002/jmor.10169 Google Scholar
  197. Vogt G, Tolley L, Scholtz G (2004) Life stages and reproductive components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. J Morphol 261:286–311.  https://doi.org/10.1002/jmor.10250 Google Scholar
  198. Vogt G, Wirkner CS, Richter S (2009) Symmetry variation in the heart-descending artery system of the parthenogenetic marbled crayfish. J Morphol 270:221–226.  https://doi.org/10.1002/jmor.10676 Google Scholar
  199. Vojkovská R, Horká I, Tricarico E, Ďuriš Z (2014) New record of the parthenogenetic marbled crayfish Procambarus fallax f. virginalis from Italy. Crustaceana 87:1386–1392.  https://doi.org/10.1163/15685403-00003365 Google Scholar
  200. Walker CH, Sibly R, Hopkin S, Peakall DB (2012) Principles of ecotoxicology. CRC Press, Boca RatonGoogle Scholar
  201. Weiperth A, Csányi B, Gál B, György ÁI, Szalóky Z, Szekeres J, Tóth B, Puky M (2015) Egzotikus rák-, hal-és kétéltűfajok a Budapest környéki víztestekben [exotic crayfish, fish and amphibian species in various water bodies in the region of Budapest]. Pisces Hungarici 9:65–70Google Scholar
  202. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666.  https://doi.org/10.2307/2265769 Google Scholar
  203. Wine J, Krasne F (1972) The organization of escape behaviour in the crayfish. J Exp Biol 56:1–18Google Scholar
  204. Yue G, Wang G, Zhu B, Wang C, Zhu Z, Lo L (2008) Discovery of four natural clones in a crayfish species Procambarus clarkii. Int J Biol Sci 4:279Google Scholar
  205. Zulandt T, Zulandt-Schneider RA, Moore PA (2008) Observing agonistic interactions alters subsequent fighting dynamics in the crayfish, Orconectes rusticus. Anim Behav 75:13–20.  https://doi.org/10.1016/j.anbehav.2007.04.017 Google Scholar

Copyright information

© Institute of Zoology, Slovak Academy of Sciences 2018

Authors and Affiliations

  1. 1.South Bohemian Research Centre of Aquaculture and Biodiversity of Hydrocenoses, Faculty of Fisheries and Protection of WatersUniversity of South Bohemia in České BudějoviceVodňanyCzech Republic
  2. 2.Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural ResourcesCzech University of Life Sciences PraguePraha - SuchdolCzech Republic

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