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Marine Biology

, Volume 149, Issue 4, pp 775–787 | Cite as

Movement patterns of the limpet Cellana grata (Gould) observed over a continuous period through a changing tidal regime

  • Mark S. DaviesEmail author
  • M. Edwards
  • Gray A. Williams
Research Article

Abstract

Time-lapse videography of limpets mounted with light-emitting diodes was used to monitor the movements of a population of the non-homing Cellana grata on a vertical gully wall in Hong Kong. Animals were monitored for >7 days to examine spatial and temporal variation in their behaviour as the tides transited from a semi-diurnal to an almost diurnal pattern. Movement was synchronised with the tides, irrespective of the day–night cycles. Limpets rested low on the shore and were stimulated to move by the rising tide. Individuals moved up shore with the flooding tide, maintaining themselves in the awash zone, and then down shore on the ebbing tide, until they reached a resting height when the tide then fell beneath them, exhibiting ‘zonal shuttling’. A tight coupling of limpet position to tide height persisted through the changing tidal pattern, and almost all animals displayed the same organisation of activity over all tides. Initiation of activity and maximum height reached were probably controlled by the tides, but the cessation of activity may have been controlled by an internal clock. The pattern observed is consistent with the threat of attack from aquatic predators coupled with the need to minimise physical stresses while exposed. It is also consistent with the avoidance of grazing lower on the shore where interspecific competition may be more intense. Limpets showed two peaks of activity per tide, corresponding to when the rate of change of tide height was the greatest, except when tides became much reduced during the transit to a diurnal pattern. Movement was triphasic: an initial rapid phase, followed by a slower phase in the high shore and then a rapid phase before the limpets stopped moving. This structure is common in limpets and in this case is likely to be a consequence of animals maintaining themselves within the awash zone. Tide height appears to determine foraging activity, but with modifications in the behaviour in response to factors operating at more local temporal and spatial scales.

Keywords

Tidal Cycle Flood Tide Diurnal Pattern Tidal Amplitude Tide Height 
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

Acknowledgements

M.D. was supported by a Wain Fellowship, BBSRC, UK. We are grateful to two anonymous referees for clarifying our thinking.

References

  1. Branch GM (1981) The biology of limpets: physical factors, energy flow and ecological interactions. Oceanogr Mar Biol Ann Rev 19:235–380Google Scholar
  2. Brown AC (1982) The biology of sandy-beach whelks of the genus Bullia (Nassaridae). Oceanogr Mar Biol Ann Rev 20:309–361Google Scholar
  3. Boyden CR, Zeldis JR (1979) Preliminary observations using an attached microphonic sensor to study feeding behaviour of an intertidal limpet. Estuar Coast Mar Sci 9:759–769CrossRefGoogle Scholar
  4. Burrows MT, Hughes RN (1989) Natural foraging of the dogwhelk, Nucella lapillus (Linnaeus)—the weather and whether to feed. J Moll Stud 55:285–295Google Scholar
  5. Chapman MG, Underwood AJ (1992) Experimental designs for analysis of movements by molluscs. In: Grahame J, Mill PJ, Reid DG (eds) Proceedings of the third international symposium on littorinid biology. The Malacological Society of London, London, pp 169–180Google Scholar
  6. Chelazzi G, Innocenti R, Della Santina P (1983) Zonal migration and trail-following of an intertidal gastropod analyzed by LED tracking in the field. Mar Behav Physiol 10:121–136Google Scholar
  7. Chelazzi G, Della Santina P, Parpagnoli D (1987) Trail following in the chiton Acanthopleura gemmata: operational and ecological problems. Mar Biol 95:539–545CrossRefGoogle Scholar
  8. Chelazzi G, Focardi S, Deneubourg J-L (1988) Analysis of movement patterns and orientation mechanisms in intertidal chitons and gastropods. In: Chelazzi G, Vannini M (eds) Behavioral adaptation to intertidal life, NATO ASI series, series a: life sciences, vol 151. Plenum Press, New York, pp 173–184Google Scholar
  9. Chelazzi G, Terranova G, Della Santina P (1990) A field technique for recording the activity of limpets. J Moll Stud 56:595–600Google Scholar
  10. Chelazzi G, Santini G, Parpagnoli D, Della Santina P (1994) Coupling motographic and sonographic recording to assess foraging behaviour of Patella vulgata. J Moll Stud 60:123–128Google Scholar
  11. Chelazzi G, Santini G, Della Santina P (1998) Route selection in the foraging of Patella vulgata (Mollusca: Gastropoda). J Mar Biol Assoc UK 78:1223–1232Google Scholar
  12. Choat JH (1977) The influence of sessile organisms on the population biology of three species of Acmaeid limpets. J Exp Mar Biol Ecol 26:1–26CrossRefGoogle Scholar
  13. Cockroft VG, Forbes AT (1981) Tidal activity rhythms in the mangrove snail Cerithidea decollata (Gastropoda, Prosobranchia, Cerithiidae). S Afr J Zool 16:5–9Google Scholar
  14. Craig PC (1968) The activity pattern and food habits of the limpet Acmaea pelta. Veliger 11(Suppl):13–19Google Scholar
  15. Davies MS, Williams GA (1995) Pedal mucus of a tropical limpet, Cellana grata (Gould): energetics, production and fate. J Exp Mar Biol Ecol 186:77–87CrossRefGoogle Scholar
  16. Della Santina P, Naylor E (1993) Endogenous rhythms in the homing behaviour of the limpet Patella vulgata Linnaeus. J Moll Stud 60:87–91Google Scholar
  17. Della Santina P, Naylor E, Chelazzi G (1994) Long-term field actography to assess the timing of foraging excursions in the limpet Patella vulgata L. J Exp Mar Biol Ecol 178:193–203CrossRefGoogle Scholar
  18. Eaton CM (1968) The activity and the food of the file limpet Acmaea limulata. Veliger 11(Suppl):5–12Google Scholar
  19. Erlandsson J, Kostylev V (1995) Trail following, speed and fractal dimension of movement in a marine prosobranch, Littorina littorea, during a mating and a non-mating season. Mar Biol 122:87–94CrossRefGoogle Scholar
  20. Erlandsson J, Kostylev V, Williams G A (1999) A field technique for estimating the influence of surface complexity on movement tortuosity in the tropical limpet Cellana grata Gould. Ophelia 50:215–224Google Scholar
  21. Evans M, Williams GA (1991) Time partitioning of foraging in the limpet Patella vulgata. J Anim Ecol 60:563–575CrossRefGoogle Scholar
  22. Frontier S (1987) Applications of fractal theory to ecology. In: Legendre P, Legendre L (eds) Developments in numerical ecology. NATO ASI Series G14, Springer, Berlin Heidelberg New York, pp 335–378Google Scholar
  23. Garrity SD (1984) Some adaptations of gastropods to physical stress on a tropical rocky shore. Ecology 65:559–574CrossRefGoogle Scholar
  24. Gray DR, Hodgson AN (1997) Temporal variation in foraging behaviour of Patella granularis (Patellogastropoda) and Siphonaria concinna (Basommatophora) on a South African shore. J Moll Stud 63:121–130Google Scholar
  25. Gray DR, Hodgson AN (1999) Endogenous rhythms of locomotor activity in the high-shore limpet, Helcion pectunculus (Patellogastropoda). Anim Behav 57:387–391CrossRefPubMedGoogle Scholar
  26. Hamilton PV (1977) Daily movements and visual location of plant stems by Littorina irrorata (Mollusca, Gastropoda). Mar Behav Physiol 4:293–304Google Scholar
  27. Harper KD, Williams GA (2001) Variation in abundance and distribution of the chiton Acanthopleura japonica and associated molluscs on a seasonal, tropical, rocky shore. J Zool 253:293–300CrossRefGoogle Scholar
  28. Hartnoll RG, Wright JR (1977) Foraging movements and homing in the limpet Patella vulgata. Anim Behav 25:806–810CrossRefGoogle Scholar
  29. Hawkins SJ, Hartnoll RG (1982) The influence of barnacle cover on the numbers, growth and behaviour of Patella vulgata L. on a vertical pier. J Mar Biol Assoc UK 62:865–867Google Scholar
  30. Hawkins SJ, Hartnoll RG (1983) Grazing of intertidal algae by marine invertebrates. Oceanogr Mar Biol Ann Rev 21:195–282Google Scholar
  31. Hazlett BA (1984) Daily movements of some tropical marine gastropods. Mar Behav Physiol 11:35–48CrossRefGoogle Scholar
  32. Hirano Y (1979a) Studies on activity pattern in the patellid limpet Cellana toreuma (Reeve). J Exp Mar Biol Ecol 40:137–148CrossRefGoogle Scholar
  33. Hirano Y (1979b) Activity pattern of the limpet, Cellana nigrolineata. Venus 38:35–47Google Scholar
  34. Hodgson AN (1999) The biology of the siphonariid limpets (Gastropoda: Pulmonata). Oceanogr Mar Biol Ann Rev 37:245–314Google Scholar
  35. Huang R (2001) Spatial variation in Cellana grata populations: the interplay of population dynamics and food availability. Unpublished PhD thesis, University of Hong KongGoogle Scholar
  36. Hutchinson N, Williams GA (2003) An assessment of variation in molluscan grazing pressure on Hong Kong rocky shores. Mar Biol 142:495–507Google Scholar
  37. Jones NS (1948) Observations and experiments on the biology of Patella vulgata at Port St. Mary, Isle of Man. Proc Trans Liverpool Biol Soc 56:60–77Google Scholar
  38. Levings SC, Garrity SD (1983) Diel and tidal Movement of 2 co-occuring Neritid snails: differences in grazing patterns on a tropical rocky shore. J Exp Mar Biol Ecol 67:261–278CrossRefGoogle Scholar
  39. Little C (1989) Factors governing patterns of foraging activity in littoral marine herbivorous molluscs. J Moll Stud 55:273–284Google Scholar
  40. Little C, Stirling P (1985) Patterns of foraging activity in the limpet Patella vulgata L.—a preliminary study. J Exp Mar Biol Ecol 89:283–296CrossRefGoogle Scholar
  41. Little C, Williams GA, Morritt D, Perrins JM, Stirling P (1988) Foraging behaviour of Patella vulgata L. in an Irish sea-lough. J Exp Mar Biol Ecol 120:1–21CrossRefGoogle Scholar
  42. Little C, Partridge JC, Teagle L (1991) Foraging activity of limpets in normal and abnormal tidal regimes. J Mar Biol Assoc UK 71:537–554CrossRefGoogle Scholar
  43. McLachlan A, Wooldridge T, Van Der Horst G (1979) Tidal movements of the macrofauna on an exposed sandy beach in South Africa. J Zool 187:433–442CrossRefGoogle Scholar
  44. Magnus DBE, Haacker U (1968) Zum phanomen der ortsunsteten ruheversammlungen der strandschnecke Planaxis sulcatus (Born) (Mollusca, Prosobranchia). Sarsia 34:137–148Google Scholar
  45. Miller AC (1968) Orientation and movement of the limpet Acmaea digitalis on vertical rock surfaces. Veliger 11(Suppl):13–19Google Scholar
  46. Morton B, Morton J. (1983) The seashore ecology of Hong Kong. Hong Kong University Press, Hong KongGoogle Scholar
  47. Nagarkar S, Williams GA (1999) Cyanobacteria dominated epilithic biofilms: spatial and temporal variation on semi-exposed tropical rocky shores. Phycologia 38:385–393CrossRefGoogle Scholar
  48. Naylor E (1988) Clock-controlled behaviour in intertidal animals. In: Chelazzi G, Vannini M (eds) Behavioral adaptation to intertidal life, NATO ASI series, series a: life sciences, vol 151. Plenum Press, New York, pp 1–14Google Scholar
  49. Orton JH (1929) Observations on Patella vulgata. Part III Habitats and habits. J Mar Biol Assoc UK 16:277–288Google Scholar
  50. Parpagnoli D, Chelazzi G (1995) An automatic technique for recording the grazing activity in limpets. J Moll Stud 61:339–346Google Scholar
  51. Rogers DA (1968) The effects of light and tide on the movement of the limpet Acmaea scutum. Veliger 11(Suppl):20–24Google Scholar
  52. Ruiz Sebastián C, Steffani CN, Branch GM (2002) Homing and movement patterns of a South African limpet Scutellastra argenvillei in an area invaded by an alien mussel Mytilus galloprovincialis. Mar Ecol Prog Ser 243:111–122Google Scholar
  53. Serra G, Chelazzi G, Castilla AC (2001) Temporal and spatial activity of the key-hole limpet Fissurella crassa (Mollusca: Gastropoda) in the eastern Pacific. J Mar Biol Assoc UK 81:485–490CrossRefGoogle Scholar
  54. Thain VM (1971) Diurnal rhythms in snails and starfish. In: Crisp DJ (ed) 4th European marine biology symposium. Cambridge University Press, Cambridge, p 513Google Scholar
  55. Thomas RF (1973) Homing behavior and movement rhythms in the pulmonate limpet Siphonaria pectinata Linnaeus. Proc Malac Soc Lond 40:303–311Google Scholar
  56. Verderber GW, Cook SB, Cook CB (1983) The role of the home scar in reducing water loss during aerial exposure of the pulmonate limpet, Siphonaria alternata (Say). Veliger 25:235–343Google Scholar
  57. Wells RA (1980) Activity pattern as a mechanism of predator avoidance in two species of acmaeid limpet. J Exp Mar Biol Ecol 48:151–168CrossRefGoogle Scholar
  58. Williams GA (1993) The relationship between herbivorous molluscs and algae on moderately exposed Hong Kong Shores. In: Morton B (ed) The marine biology of the south china sea: proceedings of the first international conference on the marine biology of Hong Kong and the South China Sea, Hong Kong 28 October–3 November 1990. Hong Kong University Press, Hong Kong, pp 459–470Google Scholar
  59. Williams GA (1994) Grazing by littorinids on a moderately exposed tropical rocky shore. In: Morton B (ed) The Malacofauna of Hong Kong and Southern China III: proceedings of the third international workshop on the Malacofauna of Hong Kong and Southern China, Hong Kong 13 April–1 May 1992. Hong Kong University Press, Hong Kong, pp 379–389Google Scholar
  60. Williams GA, Morritt D (1995) Habitat partitioning and thermal tolerance in a tropical limpet, Cellana grata. Mar Ecol Prog Ser 124:89–103Google Scholar
  61. Williams GA, Little C, Morritt D, Stirling P, Teagle L, Miles A, Pilling G, Consalvey M (1999) Foraging in the limpet Patella vulgata: the influence of rock slope on the timing of activity. J Mar Biol Assoc UK 79:881–889CrossRefGoogle Scholar
  62. Wolcott TG (1973) Physiological ecology and intertidal zonation in limpets (Acmaea): a critical look at ‘limiting factors’. Biol Bull 145:389–422Google Scholar
  63. Zar JH (1984) Biostatistical analysis. Prentice Hall, LondonGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Mark S. Davies
    • 1
    Email author
  • M. Edwards
    • 1
    • 2
  • Gray A. Williams
    • 2
  1. 1.School of Health, Natural and Social SciencesUniversity of SunderlandSunderlandUK
  2. 2.Swire Institute of Marine Science, Department of Ecology and BiodiversityThe University of Hong KongHong KongChina

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