Skip to main content
Log in

Role of the olfactory pathway in agonistic behavior of crayfish, Procambarus clarkii

  • Original Paper
  • Published:
Invertebrate Neuroscience

Abstract

Crayfish establish social dominance hierarchies through agonistic interactions, and these hierarchies are maintained through assessment of social status. Chemical signals influence several aspects of fighting behavior, but the specific chemosensory sensilla involved in detecting these signals in crayfish are unknown. The goal of our study was to examine the importance of aesthetasc sensilla—olfactory sensors on the antennules of decapod crustaceans—in regulating changes in fighting behavior in crayfish, Procambarus clarkii, over the course of repeated pairings. We selectively ablated aesthetascs from pairs of crayfish after the first day of trials and compared the behavior of these ablated animals to that of pairs of intact controls. Results show that unablated crayfish significantly decreased the number and duration of fights over repeated pairings, whereas crayfish lacking aesthetascs continued to engage in similar amounts of fighting across all three trial days. This difference shows that aesthetascs regulate fighting behavior in P. clarkii.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ache BW, Macmillan DL (1980) Neurobiology. In: Cobb JS, Phillips BF (eds) The biology and management of lobsters. Academic, New York, pp 165–213

    Google Scholar 

  • Ache BW, Young JM (2005) Olfaction: diverse species, conserved principles. Neuron 48:417–430

    Article  PubMed  CAS  Google Scholar 

  • Belanger RM, Moore PA (2006) The use of the major chelae by reproductive male crayfish (Orconectes rusticus) for discrimination of female odors. Behaviour 143:713–731

    Article  Google Scholar 

  • Bergman DA, Kozlowski CP, McIntyre JC, Huber R, Daws AG, Moore PA (2003) Temporal dynamics and communication of winner-effects in the crayfish, Orconectes rusticus. Behaviour 140:805–825

    Article  Google Scholar 

  • Breithaupt T, Atema J (1993) Evidence for the use of urine signals in agonistic interactions of the American lobster. Biol Bull 185:318

    Google Scholar 

  • Breithaupt T, Atema J (2000) The timing of chemical signaling with urine in dominance fights of male lobsters (Homarus americanus). Behav Ecol Sociobiol 49:67–78

    Article  Google Scholar 

  • Breithaupt T, Eger P (2002) Urine makes the difference: chemical communication in fighting crayfish made visible. J Exp Biol 205:1221–1231

    PubMed  Google Scholar 

  • Bruski CA, Dunham DW (1987) The importance of vision in agonistic communication of the crayfish Orconectes rusticus. I. An analysis of bout dynamics. Behaviour 103:83–107

    Google Scholar 

  • Cate HS, Derby CD (2001) Morphology and distribution of setae on the antennules of the Caribbean spiny lobster Panulirus argus reveal new types of bimodal chemo-mechanosensilla. Cell Tissue Res 304:439–454

    Article  PubMed  CAS  Google Scholar 

  • Cate HS, Derby CD (2002a) Hooded sensilla homologues: structural variations of a widely distributed bimodal chemo-mechanosensillum. J Comp Neurol 444:345–357

    Article  PubMed  Google Scholar 

  • Cate HS, Derby CD (2002b) Ultrastructure and physiology of the hooded sensillum, a bimodal chemo-mechanosensillum of lobsters. J Comp Neurol 442:293–307

    Article  PubMed  Google Scholar 

  • Chichibu S, Wada T, Komiya H (1978) Structure of mechanoreceptive hairs on the crayfish first antenna. Acta Med Kinki Univ 3:27–39

    Google Scholar 

  • Copp NH (1986) Dominance hierarchies in the crayfish Procambarus clarkii (Girard, 1852) and the question of learned individual recognition (Decapoda, Astacidea). Crustaceana 51:9–23

    Article  Google Scholar 

  • Corotto FS, O’Brien MR (2002) Chemosensory stimuli for the walking legs of the crayfish Procambarus clarkii. J Chem Ecol 28:1117–1130

    Article  PubMed  CAS  Google Scholar 

  • Derby CD (1982) Structure and function of cuticular sensilla of the lobster Homarus americanus. J Crust Biol 2:1–21

    Article  Google Scholar 

  • Dunham DW, Ciruna KA, Harvey HH (1997) Chemosensory role of antennules in the behavioral integration of feeding by the crayfish Cambarus bartonii. J Crust Biol 17:27–32

    Article  Google Scholar 

  • Eisthen HL (2002) Why are olfactory systems of different animals so similar? Brain Behav Evol 59:273–293

    Article  PubMed  Google Scholar 

  • Garm A, Hallberg E, Høeg JT (2003) Role of maxilla 2 and its setae during feeding in the shrimp Palaemon adspersus (Crustacea: Decapoda). Biol Bull 204:126–137

    Article  PubMed  CAS  Google Scholar 

  • Giri T, Dunham DW (1999) Use of the inner antennule ramus in the localisation of distant food odours by Procambarus clarkii (Girard, 1852) (Decapoda, Cambaridae). Crustaceana 72:123–127

    Google Scholar 

  • Giri T, Dunham DW (2000) Female crayfish (Procambarus clarkii (Girard, 1852)) use both antennular rami in the localization of male odour. Crustaceana 73:447–458

    Article  Google Scholar 

  • Gleeson RA (1982) Morphological and behavioral identification of the sensory structures mediating pheromone reception in the blue crab Callinectes sapidus. Biol Bull 163:162–171

    Article  Google Scholar 

  • Gleeson RA (1991) Intrinsic factors mediating pheromone communication in the blue crab, Callinectes sapidus. In: Bauer RT, Martin JW (eds) Crustacean sexual biology. Columbia University Press, New York, pp 17–32

    Google Scholar 

  • Goessmann C, Hemelrijk C, Huber R (2000) The formation and maintenance of crayfish hierarchies: behavioral and self-structuring properties. Behav Ecol Sociobiol 48:418–428

    Article  Google Scholar 

  • Grünert U, Ache BW (1988) Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster, Panulirus argus. Cell Tissue Res 251:95–103

    Article  Google Scholar 

  • Hallberg E, Johansson KUI, Elofsson R (1992) The aesthetasc concept: structural variations of putative olfactory receptor cell complexes in Crustacea. Microsc Res Tech 22:325–335

    Article  PubMed  CAS  Google Scholar 

  • Hallberg E, Johansson KUI, Wallen R (1997) Olfactory sensilla in crustaceans: morphology, sexual dimorphism, and distribution patterns. Int J Insect Morphol Embryol 26:173–180

    Article  Google Scholar 

  • Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Ann Rev Neurosci 20:595–631

    Article  PubMed  CAS  Google Scholar 

  • Holmes SJ, Homuth ES (1910) The seat of smell in the crayfish. Biol Bull 18:155–160

    Article  Google Scholar 

  • Horner AJ, Weissburg MJ, Derby CD (2008) The olfactory pathway mediates sheltering behavior of Caribbean spiny lobsters, Panulirus argus, in response to urine signals. J Comp Physiol A (in press)

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

    Article  PubMed  CAS  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 

  • Johnson ME, Atema J (2005) The olfactory pathway for individual recognition in the American lobster Homarus americanus. J Exp Biol 208:2865–2872

    Article  PubMed  Google Scholar 

  • Karavanich C, Atema J (1998a) Olfactory recognition of urine signals in dominance fights between male lobsters, Homarus americanus. Behaviour 135:719–730

    Google Scholar 

  • Karavanich C, Atema J (1998b) Individual recognition and memory in lobster dominance. Anim Behav 56:1553–1560

    Article  PubMed  Google Scholar 

  • Mellon D Jr, Tuten HR, Redick J (1989) Distribution of radioactive leucine following uptake by olfactory sensory neurons in normal and heteromorphic crayfish antennules. J Comp Neurol 280:645–662

    Article  PubMed  Google Scholar 

  • Mellon D Jr, Munger SD (1990) Nontopographic projection of olfactory sensory neurons in the crayfish brain. J Comp Neurol 296:253–262

    Article  PubMed  Google Scholar 

  • Mellon D Jr (2005) Integration of hydrodynamic and odorant inputs by local interneurons of the crayfish deutocerebrum. J Exp Biol 208:3711–3720

    Article  PubMed  Google Scholar 

  • Rutherford PL, Dunham DW, Allison V (1996) Antennule use and agonistic success in the crayfish Orconectes rusticus. Crustaceana 69:117–122

    Google Scholar 

  • Sandeman DC, Luff SE (1974) Regeneration of the antennules in the Australian freshwater crayfish, Cherax destructor. J Neurobiol 5:475–488

    Article  PubMed  CAS  Google Scholar 

  • Sandeman D, Sandeman R, Derby C, Schmidt M (1992) Morphology of the brain of crayfish, crabs, and spiny lobsters - a common nomenclature for homologous structures. Biol Bull 183:304–326

    Article  Google Scholar 

  • Sandeman R, Sandeman D (1996) Pre- and postembryonic development, growth and turnover of olfactory receptor neurones in crayfish antennules. J Exp Biol 199:2409–2418

    PubMed  Google Scholar 

  • Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct Develop 34:257–299

    Article  Google Scholar 

  • Schmidt M (1989) The hair-peg organs of the shore crab, Carcinus maenas (Crustacea, Decapoda): ultrastructure and functional properties of sensilla sensitive to changes in seawater concentration. Cell Tissue Res 257:609–622

    Article  Google Scholar 

  • Schmidt M, Ache BW (1992) Antennular projections to the midbrain of the spiny lobster. II. Sensory innervation of the olfactory lobe. J Comp Neurol 318:291–303

    Article  PubMed  CAS  Google Scholar 

  • Schmidt M, Ache BW (1993) Antennular projections to the midbrain of the spiny lobster. III. Central arborizations of motoneurons. J Comp Neurol 336:583–594

    Article  PubMed  CAS  Google Scholar 

  • Schmidt M, Ache BW (1996a) Processing of antennular input in the brain of the spiny lobster, Panulirus argus.I. Non-olfactory chemosensory and mechanosensory pathway of the lateral and median antennular neuropils. J Comp Physiol A 178:579–604

    Google Scholar 

  • Schmidt M, Ache BW (1996b) Processing of antennular input in the brain of the spiny lobster, Panulirus argus. II. The olfactory pathway. J Comp Physiol A 178:605–628

    Google Scholar 

  • Schmidt M, Derby CD (2005) Non-olfactory chemoreceptors in asymmetric setae activate antennular grooming behavior in the Caribbean spiny lobster Panulirus argus. J Exp Biol 208:233–248

    Article  PubMed  CAS  Google Scholar 

  • Schmidt M, Gnatzy W (1984) Are the funnel-canal organs the campaniform sensilla of the shore crab, Carcinus maenas (Decapoda, Crustacea) II. Ultrastructure. Cell Tissue Res 237:81–94

    Article  PubMed  CAS  Google Scholar 

  • Schmidt M, Van Ekeris L, Ache BW (1992) Antennular projections to the midbrain of the spiny lobster. I. Sensory Innervation of the lateral and median antennular neuropils. J Comp Neurol 318:277–290

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Steullet P, Cate HS, Michel WC, Derby CD (2000) Functional units of a compound nose: aesthetasc sensilla house similar populations of olfactory receptor neurons on the crustacean antennule. J Comp Neurol 418:270–280

    Article  PubMed  CAS  Google Scholar 

  • Tierney AJ, Thompson CS, Dunham DW (1986) Fine structure of aesthetasc chemoreceptors in the crayfish Orconectes propinquus. Can J Zool 64:392–399

    Google Scholar 

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

    Article  Google Scholar 

  • Zulandt Schneider RA, Huber R, Moore PA (2001) Individual and status recognition in the crayfish, Orconectes rusticus: the effects of urine release on fight dynamics. Behaviour 138:137–153

    Article  Google Scholar 

Download references

Acknowledgments

We thank Joy Tapp and Luan Vu for assistance with the behavioral trials, and Fadi Issa for helpful advice on experimental design. This work was supported by National Science Foundation grant IBN-0077474 and a grant from the Center for Behavioral Neuroscience under the STC Program of the National Science Foundation under Agreement No. IBN-9876754.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charles D. Derby.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Horner, A.J., Schmidt, M., Edwards, D.H. et al. Role of the olfactory pathway in agonistic behavior of crayfish, Procambarus clarkii . Invert Neurosci 8, 11–18 (2008). https://doi.org/10.1007/s10158-007-0063-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10158-007-0063-1

Keywords

Navigation