Advertisement

Marine Biology

, Volume 158, Issue 6, pp 1331–1337 | Cite as

Shelter selection of the spiny lobster Palinurus elephas under different levels of Octopus vulgaris predation threat

  • M. Gristina
  • M. Sinopoli
  • F. Fiorentino
  • G. Garofalo
  • F. Badalamenti
Original Paper

Abstract

The skill of recognizing and reacting to predators is often based on a learned component. Few studies have examined the role of learning in spiny lobster anti-predator behavior. We investigated whether European spiny lobster (Palinurus elephas) shelter selection is influenced by olfactory stimuli released by one of the most common lobster predators, the common octopus (Octopus vulgaris), and whether the behavioral response to octopus chemical stimuli is innate or influenced by experience. In experimental arenas, we conditioned wild-caught lobsters with three levels of predation threat: no threat, with no predator–prey interaction; medium threat, with odor and visual predator cues only; high threat, active predation risk. We subsequently tested the shelter choice of the conditioned lobster under different experimental conditions: (1) shelter plus seawater; (2) shelter plus seawater plus chemical octopus cue. Our results showed significant differences in mean shelter occupancy with conditioning level. We conclude that P. elephas individuals use chemosensory systems in predator-avoidance mechanisms. Moreover, lobsters subject to a training period of high-level predation threat were able to learn the octopus chemical stimuli and treat its odor as a cue related to predation risk. The findings relative to the spiny lobster learning abilities could be an important tool for future management of lobster populations, e.g., by re-introduction of reared juveniles, which have not yet experienced predation.

Keywords

Spiny Lobster Predation Threat Predator Odor High Threat Injured Conspecific 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank G. Cicchirillo and V. Di Stefano for their time and advice. Additionally, we thank anonymous reviewers for useful comments on the submitted version.

References

  1. Barshaw DE, Lavalli KL, Spanier E (2003) Offense versus defense: responses of three morphological types of lobsters to predation. Mar Ecol Prog Ser 256:171–182CrossRefGoogle Scholar
  2. Berger DK, Butler MJ (2001) Do octopus influence den selection by juvenile Caribbean spiny lobster? Mar Freshwater Res 25:515–522Google Scholar
  3. Bertelsen RD, Butler MJ, Herrnkind WF, Hunt JH (2009) Regional characterisation of hard-bottom nursery habitat for juvenile Caribbean spiny lobster (Panulirus argus) using rapid assessment techniques. New Zeal J Mar Fresh 43:299–312CrossRefGoogle Scholar
  4. Bouwma P (2006) Aspects of antipredation in Panulirus argus and Panulirus guttatus: behavior, morphology, and ontogeny. PhD dissertation, Florida State University, Tallahassee, FLGoogle Scholar
  5. Briones-Fourzán P (2009) Assessment of predation risk through conspecific alarm odors by spiny lobsters. Commun Integr Biol 2(4):302–304CrossRefGoogle Scholar
  6. Briones-Fourzán P, Ramirez-Zaldivar E, Lozano-Álvarez E (2008) Coexistence of congeneric spiny lobsters on coral reefs: differences in conspecific aggregation patterns and their potential antipredator benefits. Coral Reefs 27:275–287CrossRefGoogle Scholar
  7. Briones-Fourzàn P, Perez-Ortiz M, Lozano-Alvarez E (2006) Defence mechanisms and antipredator behaviour in two sympatric species of spiny lobsters, Panulirus argus and P. guttatus. Mar Biol 149:227–239CrossRefGoogle Scholar
  8. Brown C (2003) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish 4:227–234CrossRefGoogle Scholar
  9. Brown C, Day R (2002) The future of stock enhancements: bridging the gap between hatchery practice and conservation biology. Fish Fish 3:79–94CrossRefGoogle Scholar
  10. Brown GE, Godin JJ (1999) Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish. Anim Behav 57:475–481CrossRefGoogle Scholar
  11. Brown C, Laland K (2001) Social learning and life skills training for hatchery reared fish. J Fish Biol 49:471–493CrossRefGoogle Scholar
  12. Brown C, Warburton K (1997) Predator recognition and anti-predator responses in the rainbowfish, Melanotaenia eachamensis. Behav Ecol Sociobiol 41:61–68CrossRefGoogle Scholar
  13. Butler MJ, Herrnkind WF (1997) A test of recruitment limitation and the potential of artificial enhancement of spiny lobster populations in Florida. Can J Fish Aquat Sci 54:452–463CrossRefGoogle Scholar
  14. Butler MJ, Lear JA (2009) Habitat-based intraguild predation by Caribbean reef octopus Octopus briareus on juvenile Caribbean spiny lobster Panulirus argus. Mar Ecol Prog Ser 386:115–122CrossRefGoogle Scholar
  15. Butler MJ, MacDiarmid AB, Booth JD (1999) The cause and consequence of ontogenetic changes in social aggregation in New Zealand spiny lobsters. Mar Ecol Prog Ser 18:179–191CrossRefGoogle Scholar
  16. Butler MJ, Steneck RS, Herrnkind WF (2006) Juvenile and adult ecology. In: Phillips BF (ed) Lobsters biology, management, aquaculture and fisheries. Blackwell Scientific Publications, Oxford, pp 263–296CrossRefGoogle Scholar
  17. Caddy JF, Stamatopoulos C (1990) Mapping growth and mortality rates of crevices-dwelling organisms onto a perforated surfaces: The relevance of “cover” to the carrying capacity of natural and artificial habitats. Estuar Coast Shelf S 31:87–106CrossRefGoogle Scholar
  18. Ceccaldi HJ, Latrouite ED (2000) The French fisheries for the European spiny lobster Palinurus elephas. In: Phillips BF, Cobb JS, Kittaka J (eds) Spiny Lobster Management. Fishing New Book, Blackwell Scientific Publication, Oxford, pp 169–178Google Scholar
  19. Chivers DP, Smith RJE (1994) The role of experience and chemical alarm signalling in predator recognition by fathead minnows, Pimephales promelas. J Fish Biol 44:273–285CrossRefGoogle Scholar
  20. Chivers DP, Smith RJE (1998) Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5:338–352CrossRefGoogle Scholar
  21. Derby CD (2000) Learning from spiny lobsters about chemosensory coding of mixtures. Physiol Behav 69:203–209CrossRefGoogle Scholar
  22. Derby CD, Steullet P, Horner AJ, Cate HS (2001) The sensory basis of feeding behaviour in the Caribbean spiny lobster, Panulirus argus. Mar Fresh Res 52:1339–1350CrossRefGoogle Scholar
  23. Diaz D, Abello P, Semestre M (2001) Settlement and juvenile habitat of the European spiny lobster Palinurus elephas (Crustacea: Decapoda: Paluniridae) in the western Mediterranean Sea. Sci Mar 65:347–356CrossRefGoogle Scholar
  24. Díaz D, Zabala M, Linares C, Hereu B, Abelló P (2005) Increased predation of juvenile European spiny lobster (Palinurus elephas) in a marine protected area. New Zeal J Mar Fresh Res 39:447–453CrossRefGoogle Scholar
  25. Dicke M, Grostal P (2001) Chemical detection of natural enemies by arthropods: an ecological perspective. Annu Rev Ecol S 32:1–23CrossRefGoogle Scholar
  26. FAO (2008) Fishstat plus: Universal software for fishery statistical time series with the dataset “Capture production 1950–2007”: Available via DIALOG. http://www.fao.org/fi/statist/fisoft/FISHPLUS.asp
  27. Foster SA, Endler JA (1999) Thoughts on geographic variation in behaviour. In: Foster SA, Endler JA (eds) Geographic variation in behaviour. Perspectives on evolutionary mechanisms. Oxford University Press, Oxford, pp 287–307Google Scholar
  28. Gardner K, Frusher S, Mills D, Oliver M (2006) Simultaneous enhancement of rock lobster fisheries and provision of puerulus for aquaculture. Fish Res 80:122–128CrossRefGoogle Scholar
  29. Goñi R, Latrouite D (2005) Review of the biology, ecology, fisheries of Palinurus spp. species of European waters: palinurus elephas (Fabricius, 1787) and Palinurus mauritanicus (Gruvel, 1911). Cah Biol Mar 46:127–142Google Scholar
  30. Gristina M, Fiorentino F, Garofalo G, Badalamenti F (2009) Shelter preference in captive juveniles of European spiny lobster Palinurus elephas (Fabricius, 1787). Mar Biol 156:2097–2105CrossRefGoogle Scholar
  31. Harrington JJ, Semmens JM, Gardner C, Frusher SD (2006) Predation of trap-caught southern rock lobsters, Jasus edwardsii (Hutton, 1875), in tasmanian waters by the Maori octopus, Octopus maorum (Hutton, 1880): Spatial and temporal trends. Fish Res 77:10–16CrossRefGoogle Scholar
  32. Hazlett BA, McLay C (2000) Contingencies in the behaviour of the crab Heterozius rotundifrons. Anim Behav 59:965–974CrossRefGoogle Scholar
  33. Herrnkind WF, IV ButlerMJ, Hunt JH (1997) Can artificial habitats that mimic natural structures enhance recruitment of Caribbean spiny lobster? Fisheries 22:24–27Google Scholar
  34. Horner AJ, Nickles SP, Weissburg MJ, Derby CD (2006) Source and specificity of chemical cues mediating shelter preference of Caribbean spiny lobsters (Panulirus argus). Biol Bull 211:128–139CrossRefGoogle Scholar
  35. Hossaine MAR, Tanaka M, Masuda R (2003) Predator-prey interactions between hatchery reared Japanese flounder juvenile, Paralichthys olivaceus, and sandy shore crab, Mutua lunaris: daily rhythms, anti-predator conditioning and starvation. J Exp Mar Biol Ecol 267:1–14CrossRefGoogle Scholar
  36. Jachner A (2001) Anti-predator behaviour of naїve compared with experienced juvenile roach. J Fish Biol 59:1313–1322Google Scholar
  37. Jarvi T, Uglem I (1993) Predator training improves the anti-predator behavior of hatchery reared Atlantic salmon (Salmo solar) smolts. Nord J Fresh Res 68:63–71Google Scholar
  38. Kelley JL, Magurran AE (2003) Learned predator recognition and antipredator responses in fishes. Fish Fish 4:216–226CrossRefGoogle Scholar
  39. Kelley JL, Evans JP, Ramnarine IW, Magurran AE (2003) Back to school: can antipredator behaviour in guppies be enhanced through social learning? Anim Behav 65:655–662CrossRefGoogle Scholar
  40. Lear JA (2004) Strong interactions between juvenile Caribbean spiny lobster (Panulirus argus) and Caribbean reef octopus (Octopus briareus) in the Florida Keys, FL. M.S. Thesis, Old Dominion University, Norfolk, VAGoogle Scholar
  41. Magurran AE (1989) Acquired recognition of predator odour in the European minnow (Phoxinus phoxinus). Ethology 82:216–223CrossRefGoogle Scholar
  42. Masuda R, Ziemann DA (2000) Ontogenetic changes of learning capability and stress recovery in Pacific threadfin juveniles. J Fish Biol 56:1239–1247CrossRefGoogle Scholar
  43. Mills DJ, Gardner C, Johnson CR (2005) Experimental reseeding of juvenile spiny lobsters (Jasus edwardsii): comparing survival and movement of wild and naïve lobsters at multiple sites. Aquaculture 254:256–268CrossRefGoogle Scholar
  44. Nevitt G, Pentcheff ND, Lohmann KJ, Zimmer RK (2000) Den selection by the spiny lobster Panulirus argus: testing attraction to conspecifics odors in the field. Mar Ecol Prog Ser 203:225–231CrossRefGoogle Scholar
  45. Quetglas A, Reñones O, Goñi R (2001) Trophic interactions among grouper (Epinephelus marginatus), octopus (Octopus vulgaris) and red lobster (Palinurus elephas) in the Western mediterranean. C.I.E.S.M 36:310Google Scholar
  46. Raethke N, MacDiarmid AB, Montgomery JC (2004) The role of olfaction during mating in the southern temperate spiny lobster Jasus edwardsii. Horm Behav 146(3):311–318CrossRefGoogle Scholar
  47. Ratchford SG, Eggleston DB (1998) Size-and scale-dependent chemical attraction contribute to an ontogenetic shift in ontogeny. Anim Behav 56:1027–1034CrossRefGoogle Scholar
  48. Shabani S (2008) The role of chemical senses in predation, risk assessment and social behaviour of spiny lobsters. Phd. Thesis, College of Arts and Sciences Georgia State University, pp 1–175Google Scholar
  49. Svasand T (2004) Why juvenile quality and release strategies are important factors for stock enhancement and sea ranching. In: Leber KM, Kitada S, Blankenship HL, Svasand T (eds) Stock enhancement and sea ranching. Developments, pitfalls and opportunities, 2nd edn. Blackwell, Oxford, pp 61–70Google Scholar
  50. Tsukamoto K, Schiozawa S, Kogane T, Sakakura Y, Mizuta Y (1995) Onthogenic change in abilities of learning and memory in striped jack Pseudicaranx dentex. Saibai Giken 24:45–51Google Scholar
  51. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, CambridgeGoogle Scholar
  52. Weiss HM, Lozano-Alvares H, Briones-Fourzan P (2008) Circadian shelter occupancy patterns and predator—prey interactions of juvenile Caribbean spiny lobsters in a reef lagoon. Mar Biol 153:953–963CrossRefGoogle Scholar
  53. Zimmer-Faust RK, Tyre JE, Case JF (1985) Chemical attraction causing aggregation in the spiny lobster, Panulirus interruptus (Randall), and its probable ecological significance. Biol Bull 169:106–118CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • M. Gristina
    • 1
  • M. Sinopoli
    • 2
  • F. Fiorentino
    • 1
  • G. Garofalo
    • 1
  • F. Badalamenti
    • 3
  1. 1.IAMC-CNRMazara del ValloItaly
  2. 2.ISPRA STSPalermoItaly
  3. 3.IAMC-CNRTrapaniItaly

Personalised recommendations