Skip to main content
SpringerLink
Log in

Sex identification in female crayfish is bimodal

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Sex identification has been studied in several species of crustacean decapods but only seldom was the role of multimodality investigated in a systematic fashion. Here, we analyse the effect of single/combined chemical and visual stimuli on the ability of the crayfish Procambarus clarkii to identify the sex of a conspecific during mating interactions. Our results show that crayfish respond to the offered stimuli depending on their sex. While males rely on olfaction alone for sex identification, females require the combination of olfaction and vision to do so. In the latter, chemical and visual stimuli act as non-redundant signal components that possibly enhance the female ability to discriminate potential mates in the crowded social context experienced during mating period. This is one of the few clear examples in invertebrates of non-redundancy in a bimodal communication system.

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
Fig. 3

Similar content being viewed by others

References

  • Acquistapace P, Aquiloni L, Hazlett BA, Gherardi F (2002) Multimodal communication in crayfish: sex recognition during mate search by male Austropotamobius pallipes. Can J Zool 80:2041–2045

    Article  Google Scholar 

  • Ameyaw-Akumfi C, Hazlett BA (1975) Sex recognition in the crayfish Procambarus clarkii. Science 190:1225–1226

    Article  PubMed  CAS  Google Scholar 

  • Aquiloni L, Gherardi F (2008a) Assessing mate size in the red swamp crayfish Procambarus clarkii: effects of visual versus chemical stimuli. Freshw Biol 53:461–469

    Article  Google Scholar 

  • Aquiloni L, Gherardi F (2008b) Mutual mate choice in crayfish: large body size is selected by both sexes, virginity by males only. J Zool 274:171–179

    Article  Google Scholar 

  • Aquiloni L, Gherardi F (2008c) Evidence of cryptic mate choice in crayfish. Biol Lett 4:163–165

    Article  PubMed  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 

  • Atema J, Steinbach MA (2007) Chemical communication and social behaviour of the lobster Homarus americanus and other decapods. In: Duffy JE, Thiel M (eds) Evolutionary ecology of social and sexual systems. Oxford University Press, Oxford, UK, pp 116–190

    Google Scholar 

  • Bamber SD, Naylor E (1996) Chemical communication and behavioural interaction between sexually mature male and female shore crabs (Carcinus maenas). J Mar Biol Assoc UK 76:691–699

    Google Scholar 

  • Bamber SD, Naylor E (1997) Sites of release of putative sex pheromone and sexual behaviour in female Carcinus maenas (Crustacea: Decapoda). Est Coastal Shelf Sci 44:195–202

    Article  CAS  Google Scholar 

  • Bechler DL (1995) A review and prospectus of sexual and interspecific pheromonal communication in crayfish. Freshwater Crayfish 8:657–667

    Google Scholar 

  • Bouwma P, Hazlett BA (2001) Integration of multiple predator cues by the crayfish Orconectes propinquus. Anim Behav 61:771–776

    Article  Google Scholar 

  • Bushmann PJ (1999) Concurrent signals and behavioral plasticity in blue crab (Callinectes sapidus Rathbun) courtship. Biol Bull 197:63–71

    Article  Google Scholar 

  • Bushmann PJ, Atema J (1997) Shelter sharing and chemical courtship signals in the lobster Homarus americanus. Can J Fish Aquat Sci 54:647–654

    Article  Google Scholar 

  • Bushmann PJ, Atema J (2000) Chemically mediated mate location and evaluation in the lobster, Homarus americanus. J Chem Ecol 26:883–899

    Article  CAS  Google Scholar 

  • Caskey JL, Bauer RT (2005) Behavioral tests for a possible contact sex pheromone in the caridean shrimp Palaemonetes pugio. J Crust Biol 25:35–40

    Article  Google Scholar 

  • Christofferson JP (1970) Evidence for the controlled release of a crustacean sex pheromone. J Chem Ecol 4:633–639

    Article  Google Scholar 

  • Corotto FS, Bonenberger DM, Bounkeo JM, Dukas CC (1999) Antennule ablation, sex discrimination, and mating behavior in the crayfish Procambarus clarkii. J Crustacean Biol 19:708–712

    Article  Google Scholar 

  • Cowan DF (1991) The role of olfaction in courtship behavior of the American lobster Homarus americanus. Biol Bull 181:402–407

    Article  Google Scholar 

  • Cronin TW, Hariyama T (2002) Spectral sensitivity in crustacean eyes. In: Wiese K (ed) The crustacean nervous system. Springer, Berlin, pp 499–511

    Google Scholar 

  • Dawkins MS (1995) Unravelling animal behaviour. Longman, Harlow

    Google Scholar 

  • Díaz ER, Thiel M (2004) Chemical and visual communication during mate searching in rock shrimp. Biol Bull 206:134–143

    Article  PubMed  Google Scholar 

  • Dunham DW, Oh JW (1992) Chemical sex discrimination in the crayfish Procambarus clarkii: role of antennules. J Chem Ecol 18:2363–2372

    Article  Google Scholar 

  • Dunham DW, Oh JW (1996) Sex discrimination by female Procambarus clarkii (Girard, 1852) (Decapoda, Cambaridae): use of chemical and visual stimuli. Crustaceana 69:534–542

    Article  Google Scholar 

  • Forbes MRL, Pagola H, Baker RL (1992) Causes of a non-random pairing by size in the brine shrimp, Artemia salina (Crustacea: Anostroca). Oecologia 91:214–219

    Article  Google Scholar 

  • Galeotti P, Ruolini D, Fea G, Ghia D, Nardi PA, Gherardi F, Fasola M (2006) Cryptic female choice in a freshwater crayfish: females produce larger eggs for small, large-clawed males. Proc R Soc Lond B 273:1105–1110

    Article  Google Scholar 

  • Gherardi F (2006) Crayfish invading Europe: the case study of Procambarus clarkii. Mar Freshw Behav Physiol 39:175–191

    Article  Google Scholar 

  • Gherardi F, Raddi A, Barbaresi S, Salvi G (1999) Life history patterns of the red swamp crayfish, Procambarus clarkii, in an irrigation ditch in Tuscany. In: von Vaupel Klein JC, Schram FR (eds) The biodiversity crisis and Crustacea. Balkema, Rotterdam, pp 99–108

    Google Scholar 

  • Gherardi F, Renai B, Galeotti P, Rubolini D (2006) Nonrandom mating, mate choice, and male–male competition in the crayfish Austropotamobius italicus, a threatened species. Arch Hydrobiol 165:557–576

    Article  Google Scholar 

  • Goshima S, Koga T, Murai M (1996) Mate acceptance and guarding by male fiddler crabs Uca tetragonon (Herbst). J Exp Mar Biol Ecol 196:131–143

    Article  Google Scholar 

  • Guilford T, Dawkins MS (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42:1–14

    Article  Google Scholar 

  • Hazlett BA (1985) Chemical detection of sex and condition in the crayfish Orconectes virilis. J Chem Ecol 11:181–189

    Article  CAS  Google Scholar 

  • Hughes M (1996a) The function of concurrent signals: visual and chemical communication in snapping shrimp. Anim Behav 52:247–257

    Article  Google Scholar 

  • Hughes M (1996b) Size assessment via a visual signal in snapping shrimp. Behav Ecol Sociobiol 38:51–57

    Article  Google Scholar 

  • Huner JV, Barr JE (1991) Red swamp crawfish: biology and exploitation, 3rd edn. Sea Grant College Program, Baton Rouge, Louisiana

    Google Scholar 

  • Immelmann K, Beer C (1989) A dictionary of ethology. Harvard University Press, Cambridge, p 106

    Google Scholar 

  • Itagaki H, Thorp JH (1981) Laboratory experiments to determine if crayfish can communicate chemically in a flow-through system. J Chem Ecol 7:115–126

    Article  Google Scholar 

  • Kamio M, Matsunaga S, Fusetani N (2000) Studies on sex pheromones of the helmet crab, Telmessus cheiragonus 1. An assay based on precopulatory mate-guarding. Zool Sci 17:731–733

    Article  Google Scholar 

  • Kasuya E, Tsurumaki S, Kanie M (1996) Reversal of sex roles in the copulatory behavior of the imported crayfish Procambarus clarkii. J Crustacean Biol 16:469–471

    Article  Google Scholar 

  • Nobblitt SB, Payne JF, Delong M (1995) A comparative study of selected physical aspects of the eggs of the crayfish Procambarus clarkii (Girard, 1852) and P. zonangulus (Hobbs and Hobbs, 1990) (Decapoda, Cambaridae). Crustaceana 68:575–582

    Google Scholar 

  • Partan S, Marler P (1999) Communication goes multimodal. Science 283:1272–1273

    Article  PubMed  CAS  Google Scholar 

  • Partan S, Marler P (2005) Issues in the classification of multimodal communication signals. Amer Natural 166:231–245

    Article  Google Scholar 

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

    Google Scholar 

  • Quinn DGP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, p 556

    Google Scholar 

  • Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921–931

    Article  PubMed  Google Scholar 

  • Scheffer SJ, Uetz GW, Stratton GE (1996) Sexual selection, male morphology, and the efficacy of courtship signalling in two wolf spiders (Aranae: Lycosidae). Behav Ecol Sociobiol 38:17–23

    Article  Google Scholar 

  • Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioural sciences. McGraw-Hill, New York

    Google Scholar 

  • Simon JL, Moore PA (2007) Male–female communication in the crayfish Orconectes rusticus: the use of urinary signals in reproductive and non-reproductive pairings. Ethology 113:740–754

    Article  Google Scholar 

  • Sneddon LU, Huntingford FA, Taylor AC, Clare AS (2003) Female sex pheromone-mediated effects on behavior and consequences of male competition in the shore crab (Carcinus maenas). J Chem Ecol 29:55–70

    Article  PubMed  CAS  Google Scholar 

  • Snyder MJ, Ameyaw-Akumfi C, Chang ES (1993) Sex recognition and the role of urinary cues in the lobster, Homarus americanus. Mar Behav Physiol 24:101–116

    Article  Google Scholar 

  • Stebbing PD, Bentley MG, Watson GJ (2003) Mating behaviour and evidence for a female released courtship pheromone in the signal crayfish Pacifastacus leniusculus. J Chem Ecol 29:465–475

    Article  PubMed  CAS  Google Scholar 

  • Villanelli F, Gherardi F (1998) Breeding in the crayfish, Austropotamobius pallipes: mating patterns, mate choice and intermale competition. Freshwater Biol 40:305–315

    Article  Google Scholar 

  • Wisenden BD, Stacey NE (2005) Fish semiochemicals and the evolution of communication networks. In: McGregor PK (ed) Animal communication networks. Cambridge University Press, Cambridge, pp 540–567

    Google Scholar 

Download references

Acknowledgement

We are grateful to three anonymous referees for their helpful suggestions. The study complies with the Italian laws of animal treatment in research.

Author information

Authors and Affiliations

  1. Department of Evolutionary Biology, University of Florence, Via Romana 17, 50125, Florence, Italy

    Laura Aquiloni & Francesca Gherardi

  2. Department of Ecosystem and Public Health, University of Calgary, G362, 3330 Hospital Drive, NW Calgary, AB T2N 4N1, Canada

    Alessandro Massolo

Authors
  1. Laura Aquiloni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alessandro Massolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francesca Gherardi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura Aquiloni.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aquiloni, L., Massolo, A. & Gherardi, F. Sex identification in female crayfish is bimodal. Naturwissenschaften 96, 103–110 (2009). https://doi.org/10.1007/s00114-008-0458-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-008-0458-9

Keywords

Search

Navigation