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Marine Biology

, Volume 151, Issue 6, pp 2037–2051 | Cite as

Circatidal swimming behavior of brachyuran crab zoea larvae: implications for ebb-tide transport

  • Paola C. López-Duarte
  • Richard A. Tankersley
Research Article

Abstract

Larvae of the blue crab Callinectes sapidus and fiddler crab Uca pugilator are exported from estuaries and develop on the continental shelf. Previous studies have shown that the zoea-1 larvae of some crab species use selective tidal-stream transport (STST) to migrate from estuaries to coastal areas. The STST behavior of newly hatched larvae is characterized by upward vertical migration during ebb tide followed by a descent toward the bottom during flood. The objectives of the study were (1) to determine if newly hatched zoeae of U. pugilator and C. sapidus possess endogenous tidal rhythms in vertical migration that could underlie STST, (2) to determine if the rhythms persist in the absence of estuarine chemical cues, and (3) to characterize the photoresponses of zoeae to assess the impact of light on swimming behavior and vertical distribution. Ovigerous crabs with late-stage embryos were collected from June to August 2002 and maintained under constant laboratory conditions. Following hatching, swimming activity of zoeae was monitored in darkness for 72 h. U. pugilator zoeae displayed a circatidal rhythm in swimming with peaks in activity occurring near the expected times of ebb currents in the field. Conversely, C. sapidus zoeae exhibited no clear rhythmic migration patterns. When placed in a light field that simulated the underwater angular light distribution, C. sapidus larvae displayed a weak positive phototaxis at the highest light levels tested, while U. pugilator zoeae were unresponsive. Swimming behaviors and photoresponses of both species were not significantly influenced by the presence of chemical cues associated with offshore or estuarine water. These results are consistent with predictions based on species-specific differences in spawning and the proximity of hatching areas to the mouths of estuaries. U. pugilator larvae are released within estuaries near the adult habitat. Thus, ebb-phased STST behavior by zoeae is adaptive since it enhances export. Selective pressures for a tidal migration in C. sapidus larvae are likely weaker than for U. pugilator since ovigerous females migrate seaward prior to spawning and hatching occurs near inlets and in coastal waters.

Keywords

Vertical Migration Blue Crab Fiddler Crab Positive Phototaxis Maximum Entropy Spectral Analysis 
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

Funding was provided by the National Science Foundation (OCE 9901146/0096205 and OCE 0094930). We are grateful to K. Butler, P. Gravinese, and P. Pochelon for their help with the collection and maintenance of crabs and Dr. J. Cohen for his assistance with the phototaxis experiments. Dr. R. B. Forward, Jr. (Duke University Marine Laboratory) graciously provided laboratory space and technical support.

References

  1. Aguilar R, Hines AH, Wolcott TG, Wolcott DL, Kramer MA, Lipcius RN (2005) The timing and route of movement and migration of post-copulatory female blue crabs, Callinectes sapidus Rathbun, from the upper Chesapeake Bay. J Exp Mar Biol Ecol 319:117–128CrossRefGoogle Scholar
  2. Brookins KG, Epifanio CE (1985) Abundance of brachyuran larvae in a small coastal inlet over six consecutive tidal cycles. Estuaries 8:60–67CrossRefGoogle Scholar
  3. Broom DM (1979) Methods of detecting and analyzing activity rhythms. Biol Behav 1:3–18Google Scholar
  4. Brown SK, Loveland RE (1985) A calibration method to generate seasonal hatching profiles for the fiddler crabs Uca pugnax (Smith, 1887) and Uca minax (LeConte, 1855) (Decapoda: Brachyura). J Exp Mar Biol Ecol 90:27–42CrossRefGoogle Scholar
  5. Carr SD, Tankersley RA, Hench JL, Forward RB Jr, Luettich RA Jr (2004) Movement patterns and trajectories of ovigerous blue crabs Callinectes sapidus during the spawning migration. Estuar Coast Shelf Sci 60:567–579CrossRefGoogle Scholar
  6. Carr SD, Hench JL, Luettich RA, Forward RB Jr, Tankersley RA (2005) Spatial patterns in the ovigerous Callinectes sapidus spawning migration: results: results from a coupled behavioral-physical model. Mar Ecol Prog Ser 294:213–226CrossRefGoogle Scholar
  7. Chatfield C (1989) The analysis of time series: an introduction. Chapman and Hall, New YorkGoogle Scholar
  8. Christy JH (1982) Adaptive significance of semilunar cycles of larval release in fiddler crabs (Genus Uca): test of an hypothesis. Biol Bull 163:251–263CrossRefGoogle Scholar
  9. Christy JH (1986) Timing of larval release by intertidal crabs on an exposed shore. Bull Mar Sci 39:176–191Google Scholar
  10. Christy JH, Stancyk SE (1982) Timing of larval production and flux of invertebrate larvae in a well-mixed estuary. In: Kennedy V (eds) Estuarine comparisons. Academic, New York, pp 489–503CrossRefGoogle Scholar
  11. Cronin TW, Forward RB Jr (1979) Tidal vertical migration: an endogenous rhythm in estuarine crab larvae. Science 205:1020–1022CrossRefGoogle Scholar
  12. Cronin TW, Forward RB Jr (1983) Vertical migration rhythms of newly-hatched larvae of the estuarine crab, Rhithropanopeus harrisii. Biol Bull 165:139–153CrossRefGoogle Scholar
  13. Cronin TW, Forward RB Jr (1988) The visual pigments of crabs. I. Spectral characteristics. J Comp Physiol 162:463–478CrossRefGoogle Scholar
  14. DeCoursey PJ (1976) Vertical migration of larval Uca in a shallow estuary. Am Zool 16:244Google Scholar
  15. DeCoursey PJ (1979) Egg-hatching rhythms in three species of fiddler crabs. In: Naylor E, Hartnoll RG (eds) Cyclic phenomena in marine plants and animals. Pergamon Press, Oxford, pp 399–406CrossRefGoogle Scholar
  16. DeCoursey PJ (1983) Biological timing. In: Bliss DE, Mantele LH (eds) The biology of crustacea, vol. 7. Academic, New York, pp 107–162Google Scholar
  17. De Vries MC, Forward RB Jr (1989) Rhythms in larval release of the sublittoral crab Neopanope sayi and the supralittoral crab Sesarma cinereum (Decapoda: Brachyura). Mar Biol 100:241–248CrossRefGoogle Scholar
  18. De Vries MC, Epifanio CE, Dittel AI (1983) Lunar rhythms in the egg hatching of the subtidal crustacean Callinectes arcuatus Ordway (Decapoda: Brachyura). Estuar Coast Shelf Sci 17:717–724CrossRefGoogle Scholar
  19. De Vries MC, Tankersley RA, Forward RB Jr, Kirby Smith WW, Luettich RA Jr (1994) Abundance of estuarine crab larvae is associated with tidal hydrologic variables. Mar Biol 118:403–413CrossRefGoogle Scholar
  20. Dittel AI, Epifanio CE (1982) Seasonal abundance and vertical distribution of crab larvae in Delaware Bay, USA. Estuaries 5:197–202CrossRefGoogle Scholar
  21. Dowse HG, Ringo JM (1989) The search for hidden periodicities in biological time series revisted. J Theor Biol 139:487–515CrossRefGoogle Scholar
  22. Ehlinger GS, Tankersley RA (2006) Endogenous rhythms and entrainment cues of larval activity in horseshoe crab Limulus polyphemus. J Exp Mar Biol Ecol 337:205–214CrossRefGoogle Scholar
  23. Epifanio CE (1988) Dispersal strategies of two species of swimming crab on the continental shelf adjacent to Delaware Bay. Mar Ecol Prog Ser 49:243–248CrossRefGoogle Scholar
  24. Epifanio CE (1995) Transport of blue crab (Callinectes sapidus) larvae in the waters off Mid-Atlantic States. Bull Mar Sci 57:713–725Google Scholar
  25. Epifanio CE (2007) Larval biology. In: Kennedy VS, Cronin LE (eds) The blue crab Callinectes sapidus. Maryland Sea Grant, College Park, MD (in press)Google Scholar
  26. Epifanio CE, Valenti CC, Pembroke AE (1984) Dispersal and recruitment of blue crab larvae in the Delaware Bay, USA. Estuar Coast Shelf Sci 18:1–12CrossRefGoogle Scholar
  27. Epifanio CE, Little K, Rowe PM (1988) Dispersal and recruitment of fiddler crab larvae in the Delaware River estuary. Mar Ecol Prog Ser 43:181–188CrossRefGoogle Scholar
  28. Epifanio CE, Masse AK, Garvine RW (1989) Transport of blue crab larvae by surface currents off Delaware Bay, USA. Mar Ecol Prog Ser 54:35–41CrossRefGoogle Scholar
  29. Forward RB Jr (1977) Occurrence of a shadow response among brachyuran larvae. Mar Biol 39:331–341CrossRefGoogle Scholar
  30. Forward RB Jr (1987) Larval release rhythms of decapod crustaceans: an overview. Bull Mar Sci 41:165–176Google Scholar
  31. Forward RB Jr, Buswell CU (1989) A comparative study of behavioural responses of larval decapod crustaceans to light and pressure. Mar Behav Physiol 16:43–56CrossRefGoogle Scholar
  32. Forward RB Jr, Cronin TW (1979) Spectral sensitivity of larvae from intertidal crustacean. J Comp Physiol 133A:311–315CrossRefGoogle Scholar
  33. Forward RB Jr, Cronin TW (1980) Tidal rhythms in activity and phototaxis by an estuarine crab larva. Biol Bull 158:295–303CrossRefGoogle Scholar
  34. Forward RB Jr, Rittschof D (1994) Photoresponses of crab megalopae in offshore and estuarine waters: implications for transport. J Exp Mar Biol Ecol 182:183–192CrossRefGoogle Scholar
  35. Forward RB Jr, Tankersley RA (2001) Selective tidal-stream transport of marine animals. Oceanogr Mar Biol Ann Rev 39:305–353Google Scholar
  36. Forward RB Jr, Cronin TW, Stearns DE (1984) Control of diel vertical migration: photoresponses of a larval crustacean. Limnol Oceanogr 29:146–154CrossRefGoogle Scholar
  37. Forward RB Jr, Frankel DAZ, Rittschof D (1994) Molting of megalopae from the blue crab Callinectes sapidus: effects of offshore and estuarine cues. Mar Ecol Prog Ser 113:55–59CrossRefGoogle Scholar
  38. Forward RB Jr, Tankersley RA, Pochelon PN (2003) Circatidal activity rhythms in ovigerous blue crabs, Callinectes sapidus: implications for ebb-tide transport during the spawning migration. Mar Biol 142:67–76CrossRefGoogle Scholar
  39. Garrison LP (1999) Vertical migration behavior and larval transport in brachyuran crabs. Mar Ecol Prog Ser 176:103–113CrossRefGoogle Scholar
  40. Gibson RN (2003) Go with the flow: tidal migration in marine animals. Hydrobiologia 503:153–161CrossRefGoogle Scholar
  41. Hough AR, Naylor E (1992) Endogenous rhythms of circatidal swimming activity in estuarine copepod Eurytemora affinis (Poppe). J Exp Mar Biol Ecol 161:27–32CrossRefGoogle Scholar
  42. Lambert R, Epifanio CE (1982) A comparison of dispersal strategies in two genera of brachyuran crab in a secondary estuary. Estuaries 5:182–188CrossRefGoogle Scholar
  43. Levine J, Funes P, Dowse H, Hall J (2002) Signal analysis of behavioral and molecular cycles. Biomed Central Neurosci 3:1Google Scholar
  44. Lochmann SE, Darnell RM, McEachran JD (1995) Temporal and vertical distribution of crab larvae in a tidal pass. Estuaries 18:255–263CrossRefGoogle Scholar
  45. McConaugha JR (1988) Export and reinvasion of larvae as regulators of estuarine decapod populations. Am Fish Soc Symp 3:90–103Google Scholar
  46. McConaugha JR, Johnson DF, Provenzano AJ, Maris RC (1983) Seasonal distribution of larvae of Callinectes sapidus (Crustacea: Decapoda) in the waters adjacent to Chesapeake Bay. J Crust Biol 3:582–591CrossRefGoogle Scholar
  47. Morgan SG (1995) The timing of larval release. In: McEdward LR (ed) The ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 157–191Google Scholar
  48. Naylor E (1996) Crab clockwork: the case for interactive circatidal and circadian oscillators controlling rhythmic locomotor activity of Carcinus maenas. Chronobiol Int 13:153–161CrossRefGoogle Scholar
  49. Naylor E (2006) Orientation and navigation in coastal and estuarine zooplankton. Mar Fresh Behav Physiol 39:13–24CrossRefGoogle Scholar
  50. O’Connor NJ (1990) Morphological differentiation and molting of juvenile fiddler crabs (Uca pugilator and U. pugnax). J Crustacean Biol 10:608–612CrossRefGoogle Scholar
  51. Palmer JD (1995) The biological rhythms and clocks of intertidal animals. Oxford University Press, New YorkGoogle Scholar
  52. Pochelon PN (2005) Entrainment of circatidal activity rhythms in ovigerous blue crabs, Callinectes sapidus, and effectiveness of selective tidal-stream transport. Master’s Thesis, Florida Institute of Technology, Melbourne, FLGoogle Scholar
  53. Potvin C, Lechowicz MJ, Tardif S (1990) The statistical analysis of ecophysiological response curves obtained from experiments involving repeated measures. Ecology 71:1389–1400CrossRefGoogle Scholar
  54. Provenzano AJ Jr, McConaugha JR, Philips KB, Johnson DF, Clark J (1983) Vertical distribution of first stage larvae of the blue crab, Callinectes sapidus, at the mouth of Chesapeake Bay. Estuar Coast Shelf Sci 16:489–499CrossRefGoogle Scholar
  55. Queiroga H, Blanton J (2005) Interactions between behaviour and physical forcing in control of horizontal transport of decapod crustacean larvae. Adv Mar Biol 47:107–214CrossRefGoogle Scholar
  56. Queiroga HJ, Costlow JD, Morieira MH (1994) Larval abundance patterns of Carcinus maenas (Decapoda, Brachyura) in Canal de Mira (Ria de Aveiro, Portugal). Mar Ecol Prog Ser 111:63–72CrossRefGoogle Scholar
  57. Queiroga HJ, Costlow JD, Moreira MH (1997) Vertical migration of the crab Carcinus maenus first zoeae in an estuary: implications for tidal stream transport. Mar Ecol Prog Ser 149:121–132CrossRefGoogle Scholar
  58. Rodriguez A, Drake P, Arias AM (1997) Reproductive periods and larval abundance patterns of the crabs Panopeus africanus and Uca tangeri in a shallow inlet (SW Spain). Mar Ecol Prog Ser 149:133–142CrossRefGoogle Scholar
  59. Rosenthal R, Rosnow RL (1985) Contrast analysis: focused comparisons in the analysis of variance. Cambridge University Press, New YorkGoogle Scholar
  60. Salmon M, Seiple WH, Morgan SG (1986) Hatching rhythms of fiddler crabs and associated species at Beaufort, North Carolina. J Crustacean Biol 6:24–36CrossRefGoogle Scholar
  61. Sandifer PA (1972) Morphology and ecology of Chesapeake Bay decapod crustacean larvae. Ph.D. dissertation, University of Virginia, Charlottesville, VAGoogle Scholar
  62. Sandifer PA (1975) The role of pelagic larvae in recruitment to populations of adult decapod crustaceans in the York River estuary and adjacent lower Chesapeake Bay, Virginia. Estuar Coast Shelf Sci 3:269–279CrossRefGoogle Scholar
  63. Sulkin SD (1984) Behavioral basis of depth regulation in the larvae of brachyuran crabs. Mar Ecol Prog Ser 15:181–205CrossRefGoogle Scholar
  64. Sulkin SD, Phillips I, van Heukelem WF (1979) On the locomotory rhythm of brachyuran crab larvae and its significance in vertical migration. Mar Ecol Prog Ser 1:331–335CrossRefGoogle Scholar
  65. Sulkin SD, van Heukelem W, Kelly P, van Heukelem L (1980) The behavioral basis of larval recruitment in the crab Callinectes sapidus Rathbun: a laboratory investigation of ontogentic changes in geotaxis and barokinesis. Biol Bull 159:402–417CrossRefGoogle Scholar
  66. Tankersley RA, Forward RB Jr (1994) Endogenous activity rhythms in two estuarine crab megalopae: implications for flood tide transport. Mar Biol 118:415–424CrossRefGoogle Scholar
  67. Tankersley RA, McKelvey LM, Forward RB Jr (1995) Responses of estuarine crab megalopae to pressure, salinity and light: implications for flood-tide transport. Mar Biol 122:391–400CrossRefGoogle Scholar
  68. Tankersley RA, Wieber MG, Sigala MA, Kachurak K (1998) Migratory movements of ovigerous blue crabs, Callinectes sapidus: evidence for selective tidal-stream transport. Biol Bull 195:168–173CrossRefGoogle Scholar
  69. Turner HV, Wolcott DL, Wolcott TG, Hines AH (2003) Post-mating behavior, intramolt growth, and onset of migration to Chesapeake Bay spawning grounds by adult female blue crabs, Callinectes sapidus Rathbun. J Exp Mar Biol Ecol 295:107–130CrossRefGoogle Scholar
  70. Wheeler DE (1978) Semilunar hatching periodicity in the mud fiddler crab Uca pugnax (Smith). Estuaries 1:268–269CrossRefGoogle Scholar
  71. Young CM (1995) Behaviour and locomotion during the dispersal phase of larval life. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC, Boca Raton, FL, pp 249–277Google Scholar
  72. Zeng C, Naylor E (1996a) Synchronization of endogenous tidal vertical migration rhythms in laboratory-hatched larvae of the crab Carcinus maenas. J Exp Mar Biol Ecol 198:269–289CrossRefGoogle Scholar
  73. Zeng C, Naylor E (1996b) Endogenous tidal rhythms of vertical migration in field collected zoea-1 larvae of the shore crab Carcinus maenas: implications for ebb-tide offshore dispersal. Mar Ecol Prog Ser 132:71–82CrossRefGoogle Scholar
  74. Zeng C, Naylor E (1996c) Heritability of circatidal vertical migration rhythms in zoea larvae of the crab Carcinus maenas (L.) J Exp Mar Biol Ecol 202:239–257CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Paola C. López-Duarte
    • 1
  • Richard A. Tankersley
    • 1
  1. 1.Department of Biological SciencesFlorida Institute of TechnologyMelbourneUSA

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