Skip to main content
SpringerLink
Log in

Still waters run deep: marbled crayfish dominates over red swamp crayfish in agonistic interactions

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

Abstract

Intra- and interspecific interactions contribute to the successful establishment and consequent spreading of species in the environment, which became particularly apparent in the context of ongoing biological invasions. The parthenogenetic marbled crayfish, Procambarus virginalis, Lyko 2017 is recently recognized as an emerging invader due to its high adaptability, fast growth, early maturation, and high fecundity. The present study explored the interaction patterns of size-matched (including 15 body parts morphometry evaluation) pairs of marbled crayfish and red swamp crayfish Procambarus clarkii, a well-known highly aggressive and widely distributed invader of freshwater ecosystems. Despite this, marbled crayfish won significantly more fights and establish dominancy in more cases in both premature and mature experimental trials. Premature red swamp crayfish pairs were more active in contact and fight initiation than mature. In mature, the dominance over female red swamp crayfish was 100%, in males it reached 60%. Premature marbled crayfish dominated in more than 75% pairs. Agonistic behaviour and intensity of fights significantly dropped after establishment of dominance in particular (size and sex) pairs. Therefore, we confirmed that sex and age (size) have effects on agonistic behaviour in crayfish as well as the dominance of marbled crayfish within similarly sized specimens. Despite described behavioural patterns, we can expect that the situation in the potential sympatric occurrence of both species will not be as clear as found in experimental conditions due to greater maximal size of red swamp crayfish.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aquiloni L, Gherardi F (2008) Extended mother-offspring relationships in crayfish: the return behaviour of juvenile Procambarus clarkii. Ethol 114:946–954

    Article  Google Scholar 

  • Aquiloni L, Buřič M, Gherardi F (2008) Crayfish females eavesdrop on fighting males before choosing the dominant mate. Curr Biol 18:462–463

    Article  CAS  Google Scholar 

  • Bergman DA, Moore PA (2005) The role of chemical signals in the social behavior of crayfish. Chem Senses 30:305–306

    Article  CAS  Google Scholar 

  • Bergman DA, Martin AL, Moore PA (2005) Control of information flow through the influence of mechanical and chemical signals during agonistic encounters by the crayfish, Orconectes rusticus. Anim Behav 70:485–496

    Article  Google Scholar 

  • Bohman P, Edsman L, Martin P, Scholtz G (2013) The first Marmorkrebs (Decapoda: Astacida: Cambaridae) in Scandinavia. BioInvasion Rec 2:227–232. https://doi.org/10.3391/bir.2013.2.3.09

    Article  Google Scholar 

  • Bovbjerg RV (1953) Dominance order in the crayfish Orconectes virilis (Hagen). Physiol Zool 26:173–178

    Article  Google Scholar 

  • Bovbjerg RV (1956) Some factors affecting aggressive behavior in crayfish. Physiol Zool 29:127–136

    Article  Google Scholar 

  • Breithaupt T, Eger P (2002) Urine makes the difference. J Exp Biol 205:1221–1231

    PubMed  Google Scholar 

  • Buřič M, Kouba A, Kozák P (2010) Intra-sex dimorphism in crayfish females. Zoology 113:301–307

    Article  PubMed  Google Scholar 

  • Buřič M et al (2018) Environmentally relevant concentrations of tramadol and citalopram alter behaviour of an aquatic invertebrate. Aquat Toxicol 200:226–232

    Article  CAS  PubMed  Google Scholar 

  • Chucholl C (2015) Marbled crayfish gaining ground in Europe: the role of the pet trade as invasion pathway. In: Tadashi Kawai ZF, Scholtz G (eds) Freshwater crayfish: a global overview. CRC Press, New York, pp 83–114

    Chapter  Google Scholar 

  • 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 Inavasions 7:511–519

    Article  Google Scholar 

  • Draud M, Macías-Ordóñez R, Verga J, Itzkowitz M (2004) Female and male Texas cichlids (Herichthys cyanoguttatum) do not fight by the same rules. Behav Ecol 15:102–108

    Article  Google Scholar 

  • Duckworth RA (2008) Adaptive dispersal strategies and the dynamics of a range expansion. Am Nat 172:4–17

    Article  Google Scholar 

  • Edwards DH, Fricke RA, Barnett LD, Yeh S-R, Leise EM (1994a) The onset of response habituation during the growth of the lateral giant neuron of crayfish. J Neurophysiol 72:890–898

    Article  CAS  PubMed  Google Scholar 

  • Edwards DH, Yeh S-R, Barnett LD, Nagappan PR (1994b) Changes in synaptic integration during the growth of the lateral giant neuron of crayfish. J Neuophysiol 72:899–908

    Article  CAS  Google Scholar 

  • Estonian Research Council (2018) Invasive marbled crayfish found in Narva power plant cooling canal. https://phys.org/news/2018-06-invasive-marbled-crayfishnarva-power.html. Accessed 8 June 2018

  • 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 Rhythms 24:64–72

    Article  PubMed  Google Scholar 

  • Faulkes Z, Feria TP, Muñoz J (2012) Do marmorkrebs, Procambarus fallax f. virginalis, threaten freshwater Japanese ecosystems? Aquat Biosyst 8:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Fort M, Hossain MS, Kouba A, Buric M, Kozak P (2019) Agonistic interactions and dominance establishment in three crayfish species non-native to Europe. Limnologica 74:73–79

    Article  Google Scholar 

  • Gherardi F (2002) Behavior. In: Holdich DM (ed) Biology of Freshwater Crayfish. Blackwell Science, Oxford, pp 258–290

    Google Scholar 

  • Gherardi F, Cioni A (2004) Agonism and interference competition in freshwater decapods. Behaviour 141:1297–1324

    Article  Google Scholar 

  • Gherardi F, Daniels WH (2004) Agonism and shelter competition between invasive and indigenous crayfish species. Can J Zool 82:1923–1932

    Article  Google Scholar 

  • Herberholz J, McCurdy C, Edwards DH (2007) Direct benefits of social dominance in juvenile crayfish. Biol Bull 213:21–27

    Article  PubMed  Google Scholar 

  • Höjesjö J, Johnsson JI, Petersson E, Järvi T (1998) The importance of being familiar: individual recognition and social behavior in sea trout (Salmo trutta). Behav Ecol 9:445–451

    Article  Google Scholar 

  • Holdich D, Haffner P, Noël P (2006) Species files. In: Souty-Grosset C, Holdich D, Noel PY, Reynolds JD, Haffner P (eds) Atlas of crayfish in Europe, vol 64. Muséum national d’Histoire naturelle, Paris Patrimoines naturels, Paris, pp 50–129

    Google Scholar 

  • Holdich D, Reynolds J, Souty-Grosset C, Sibley P (2009) A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowl Manag Aquat Ecosyst 11:394–395

    Google Scholar 

  • Hossain MS, Patoka J, Kouba A, Buřič M (2018) Clonal crayfish as biological model: a review on marbled crayfish. Biologia 73:841–855. https://doi.org/10.2478/s11756-018-0098-2

    Article  Google Scholar 

  • Huber R, Kravitz E (1995) A quantitative analysis of agonistic behavior in juvenile American lobsters (Homarus americanus L.). Brain Behav Evol 46:72–83

    Article  CAS  PubMed  Google Scholar 

  • Hudina S, Hock K (2012) Behavioural determinants of agonistic success in invasive crayfish. Behav Processes 91:77–81

    Article  PubMed  Google Scholar 

  • Hudina S, Galić N, Roessink I, Hock K (2011) Competitive interactions between co-occurring invaders: identifying asymmetries between two invasive crayfish species. Biol Invasions 13:1791–1803

    Article  Google Scholar 

  • Hudina S, Hock K, Radović A, Klobučar G, Petković J, Jelić M, Maguire I (2016) Species-specific differences in dynamics of agonistic interactions may contribute to the competitive advantage of the invasive signal crayfish (Pacifastacus leniusculus) over the native narrow-clawed crayfish (Astacus leptodactylus). Mar Freshw Behav Physiol 49:147–157

    Article  Google Scholar 

  • Huntingford FA (2013) Animal conflict. Chapman & Hall Animal Behaviour Series. Springer, New York

    Google Scholar 

  • Issa FA, Adamson DJ, Edwards DH (1999) Dominance hierarchy formation in juvenile crayfish Procambarus clarkii. J Exp Biol 202:3497–3506

    PubMed  Google Scholar 

  • Janský V, Mutkovič A (2010) Rak Procambarus sp. (Crustacea: Decapoda: Cambaridae)–Prvŷ Nález na Slovensku. Acta Rerum Naturalium Musei Nationalis Slovaci Bratislava 56:64–67

    Google Scholar 

  • Jimenez SA, Faulkes Z (2010) Establishment and care of a colony of parthenogenetic marbled crayfish, Marmorkrebs. Invertebr Rearing 1:10–18

    Google Scholar 

  • Jimenez SA, Faulkes Z (2011) Can the parthenogenetic marbled crayfish Marmorkrebs compete with other crayfish species in fights? J Ethol 29:115–120

    Article  Google Scholar 

  • Jones JP et al (2009) The perfect invader: a parthenogenic crayfish poses a new threat to Madagascar’s freshwater biodiversity. Biol Invasions 11:1475–1482

    Article  Google Scholar 

  • Kasuya A, Nagayama T (2016) Habituation of Backward Escape Swimming in the Marbled Crayfish. Zool Sci 33:6–12

    Article  PubMed  Google Scholar 

  • Kawai T, Takahata M (eds) (2010) Biology of crayfish. Hokkaido University Press, Sapporo, Japan

    Google Scholar 

  • Kawai T, Faulkes Z, Scholtz G (2016) Freshwater crayfish: a global overview. CRC Press, New York

    Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  Google Scholar 

  • Kouba A et al (2016) The significance of droughts for hyporheic dwellers: evidence from freshwater crayfish. Sci Rep 6:1–7

    Article  CAS  Google Scholar 

  • Kravitz EA (1988) Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. Science 241:1775–1781

    Article  CAS  PubMed  Google Scholar 

  • Lang F, Govind C, Costello WJ, Greene SI (1977) Developmental neuroethology: changes in escape and defensive behavior during growth of the lobster. Science 197:682–685

    Article  CAS  PubMed  Google Scholar 

  • Lindqvist OV, Huner J (1999) Life history characteristics of crayfish: What makes some of them good colonizers? In: Gherardi F, Holdich DM (eds) Crayfish in Europe as Alien Species: How to make the best of the bad situation?. A. A Balkema, Rotterdam, pp 23–30

    Google Scholar 

  • Linzmaier SM, Goebel LS, Ruland F, Jeschke JM (2018) Behavioral differences in an over-invasion scenario: marbled vs. spiny-cheek crayfish. Ecosphere 9:e02385

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Manning A, Dawkins MS (2012) An introduction to animal behaviour, 5th edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Martin P, Kohlmann K, Scholtz G (2007) The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring. Naturwissenschaften 94:843–846

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Momohara Y, Kanai A, Nagayama T (2013) Aminergic control of social status in crayfish agonistic encounters. PLoS One 8:e74489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Novitsky RA, Son MO (2016) The first records of Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis](Crustacea, Decapoda, Cambaridae) in Ukraine. Ecol Monten 5:44–46

    Google Scholar 

  • Parker GA (1974) Assessment strategy and the evolution of fighting behaviour. J Theor Biol 47:223–243

    Article  CAS  PubMed  Google Scholar 

  • Pârvulescu L, Togor A, Lele S-F, Scheu S, Şinca 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

    Article  Google Scholar 

  • Patoka J et al (2016) Predictions of marbled crayfish establishment in conurbations fulfilled: evidences from the Czech Republic. Biologia 71:1380–1385

    Article  CAS  Google Scholar 

  • Pavey C, Fielder D (1996) The influence of size differntial on agonistic behaviour in the freshwater crayfish, Cherax cuspidatus (Decapoda: Parastacidae). J Zool 238:445–457

    Article  Google Scholar 

  • Reynolds J (2002) Growth and reproduction. In: Holdich DM (ed) Biology of freshwater crayfish. Blackwell Science, Oxford, pp 152–191

    Google Scholar 

  • Rubenstein DI, Hazlett BA (1974) Examination of the agonistic behaviour of the crayfish Orconectes virilis by character analysis. Behaviour 50:193–215

    Article  Google Scholar 

  • Rutherford P, Dunham D, Allison V (1996) Antennule use and agonistic success in the crayfish Orconectes rusticus (Girard, 1852) (Decapoda, Cambaridae). Crustaceana 69:117–122

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Sato D, Nagayama T (2012) Development of agonistic encounters in dominance hierarchy formation in Juvenile crayfish. J Exp Biol 215:1210–1217

    Article  PubMed  Google Scholar 

  • Schneider RAZ, Schneider RW, Moore PA (1999) Recognition of dominance status by chemoreception in the red swamp crayfish, Procambarus clarkii. J Chem Ecol 25:781–794

    Article  CAS  Google Scholar 

  • Scholtz G et al (2003) Ecology: parthenogenesis in an outsider crayfish. Nature 421:806

    Article  CAS  PubMed  Google Scholar 

  • Schroeder L, Huber R (2001) Fight strategies differ with size and allometric growth of claws in crayfish, Orconectes rusticus. Behaviour 138:1437–1449

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Shine R (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q Rev Biol 64:419–461

    Article  CAS  Google Scholar 

  • Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289

    Article  Google Scholar 

  • Smith MR, Dunham DW (1996) Antennae mediate agonistic physical contact in the crayfish Orconectes rusticus (Girard, 1852) (Decapoda, Cambaridae). Crustaceana 69:668–674

    Article  Google Scholar 

  • Souty-Grosset C, Holdich DM, Noël PY (2006) Atlas of crayfish in Europe. Collection patrimoines naturels. Muséum national d’histoire naturelle, Paris

    Google Scholar 

  • 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 Manag Inland Waters 58:78–93

    Article  Google Scholar 

  • Steele AN, Belanger RM, Moore PA (2018) Exposure through runoff and ground water contamination differentially impact behavior and physiology of crustaceans in fluvial systems. Arch Environ Contam Toxicol 75:436–448

    Article  CAS  PubMed  Google Scholar 

  • Stein RA (1976) Sexual dimorphism in crayfish chelae: functional significance linked to reproductive activities. Can J Zool 54:220–227

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179

    Google Scholar 

  • Veselý L, Buřič M, Kouba A (2015) Hardy exotics species in temperate zone: can “warm water” crayfish invaders establish regardless of low temperatures? In: Scientific reports 5

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vye C, Cobb J, Bradley T, Gabbay J, Genizi A, Karplus I (1997) Predicting the winning or losing of symmetrical contests in the American lobster Homarus americanus (Milne-Edwards). J Exp Mar Biol Ecol 217:19–29

    Article  Google Scholar 

  • Whitehouse ME (1997) Experience influences male–male contests in the spider Argyrodes antipodiana (Theridiidae: Araneae). Anim Behav 53:913–923

    Article  Google Scholar 

  • Wilson JD (1992) Correlates of agonistic display by great tits Parus major. Behaviour 121:168–214

    Article  Google Scholar 

  • Wilson EO (2000) Sociobiology. 25th Anniversary Edition edn. Harvard University Press, Cambridge

  • Wofford SJ (2013) Sex and fighting: male and female crayfish utilize different assessment strategies during agonistic behavior. Bowling Green State University, Bowling Green

    Google Scholar 

Download references

Acknowledgements

The study was financially supported by the 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) and by the Grant Agency of University of South Bohemia Nos. 012/2016/Z and 017/2016/Z. We also deeply appreciate the assistance of Dr. Zen Faulkes and for his valuable comments during manuscript preparation.

Author information

Authors and Affiliations

  1. Faculty of Fisheries and Protection of Waters, South Bohemian Research Centre of Aquaculture and Biodiversity of Hydrocenoses, University of South Bohemia in České Budějovice, Zátiší 728/II, Vodňany, 389 25, Czech Republic

    Md Shakhawate Hossain, Jan Kubec, Antonín Kouba, Pavel Kozák & Miloš Buřič

Authors
  1. Md Shakhawate Hossain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jan Kubec
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antonín Kouba
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pavel Kozák
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miloš Buřič
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Md Shakhawate Hossain.

Additional information

Handling Editor: Télesphore Sime-Ngando.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hossain, M.S., Kubec, J., Kouba, A. et al. Still waters run deep: marbled crayfish dominates over red swamp crayfish in agonistic interactions. Aquat Ecol 53, 97–107 (2019). https://doi.org/10.1007/s10452-019-09675-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-019-09675-7

Keywords

Search

Navigation