Mar Biol (2007) 151:2037–2051 DOI 10.1007/s00227-007-0614-3
R E S E A R C H A RT I C L E
Circatidal swimming behavior of brachyuran crab zoea larvae: implications for ebb-tide transport Paola C. Lo´pez-Duarte Æ Richard A. Tankersley
Received: 13 October 2006 / Accepted: 21 December 2006 / Published online: 15 March 2007 Springer-Verlag 2007
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
Communicated by J.P. Grassle. P. C. Lo´pez-Duarte (&) R. A. Tankersley Department of Biological Sciences, Florida Institute of Technology, Melbourne, FL, USA e-mail:
[email protected]
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.
Introduction Larval stages of many estuarine crabs are known to undergo development in coastal waters before reinvading and settling in juvenile nursery areas as megalopae (post-larvae). The presence of both estuarine and coastal life history stages make them ideal models for examining the roles of various physical and biological processes in dispersal, migration, and recruitment (see Forward Jr and Tankersley 2001; Naylor 2006 for reviews). For species that spawn in estuaries and undergo development in high-salinity waters of lower estuarine and shelf areas, transport seaward and through inlets is often facilitated by tidal currents. Zoeae are typically synchronously released near the time of high tide (e.g., DeCoursey 1979; Provenzano Jr et al. 1983; Christy 1986; Salmon et al. 1986; Forward
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Jr 1987; De Vries and Forward Jr 1989; Tankersley et al. 2006, Submitted). Once in the water column, they remain near the surface and are dispersed seaward by strong ebb currents (e.g., Wheeler 1978; Christy 1982; Christy and Stancyk 1982; Dittel and Epifanio 1982; Lambert and Epifanio 1982; McConaugha et al. 1983; Provenzano Jr et al. 1983; Epifanio et al. 1984, 1989; Sulkin 1984). Transport and eventual export from the estuary may be further facilitated by the coupling of vertical migration with the phasing of tidal currents, a behavioral mechanism referred to as selective tidalstream transport (STST) (see Forward Jr and Tankersley 2001; Gibson 2003 for reviews). During STST, organisms take advantage of shear flow associated with tidal currents by ascending into the water column during one phase of the tide and descending and remaining on or near the bottom during the alternate phase. During this migration, organisms are subjected to tidal currents of different intensities along the vertical shear gradient caused by the slowing of currents near the bottom by friction. Migration in synchrony with the tidal cycle results in net saltatory transport in a particular direction. Vertical ascents during ebb tides that result in seaward displacement are typically referred to as ebb-tide transport (ETT). Alternatively, flood-phased vertical migrations (i.e., flood tide transport; FTT) have been reported for a wide-range of invertebrate and fish species that utilize STST to reinvade estuaries after undergoing early development in shelf waters (Forward Jr and Tankersley 2001). The coupling of upward movement into the water column with the oscillatory flow of tidal currents could result from responses to environmental factors associated with the tides (e.g., changes in salinity, pressure, temperature, or turbulence) or an endogenous rhythm in activity (see Forward Jr and Tankersley 2001 for review). Circatidal rhythms in vertical migration that serve as estuary retention or reinvasion mechanisms have been reported in only a few invertebrate plankton species, including the copepod Eurytemora affinis (Hough and Naylor 1992), zoeae of the crab Rhithropanopeus harrisii (Cronin and Forward Jr 1979, 1983; Forward Jr and Cronin 1980) and megalopae of the fiddler crabs Uca spp. (Tankersley and Forward Jr 1994). Endogenous control of tidal migration rhythms for transport seaward in ebbing tidal flows has been reported for zoeae of the shore crab Carcinus maenas (Zeng and Naylor 1996a, b, c) and trilobite larvae of the horseshoe crab Limulus polyphemus (Ehlinger and Tankersley 2006). The use of ETT behaviors by newly hatched larvae for enhancing export from estuaries likely depends
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upon the distance of adult spawning grounds from offshore development areas. If spawning occurs near inlets, larvae may be rapidly flushed from the estuary and ETT behaviors would have little adaptive value. For example, just prior to larval release, ovigerous blue crabs Callinectes sapidus use ETT to migrate toward the entrances of estuaries and spawn in lower estuarine and coastal areas (Tankersley et al. 1998, 2006, Submitted; Carr et al. 2004). Larvae are released near the time of high tide and likely reach suitable offshore habitat within a single tidal cycle (Tankersley et al. 1998, 2006, Submitted; Carr et al. 2005). However others, including the fiddler crab Uca pugilator, release larvae near the adult habitat, which is distributed throughout estuaries. Since berried crabs do not migrate down-estuary to spawn, ETT behaviors lasting several tidal cycles would be adaptive since they would enhance down-stream transport and increase the probability of export from the estuary (Pochelon 2005; Naylor 2006). However, since tidally timed vertical migrations are energetically costly and lack apparent ecological significance in shelf waters, they should stop once larvae are beyond the influence of tidal currents associated with the estuary. The objective of the present study was to determine whether newly hatched larvae (zoea-1) of two common estuarine crabs, the fiddler crab U. pugilator and the blue crab C. sapidus, exhibit endogenously controlled rhythms in vertical migration that facilitate rapid transport in tidal currents to offshore development areas. The predicted pattern for ETT is that zoeae should exhibit maximum activity and upward swimming during periods of expected ebb tides and minimal activity and downward movement during flood tides. Since the adaptive value and ecological significance of tidal vertical migrations in estuarine areas would be lost in offshore areas, we also tested the hypothesis that circatidal swimming rhythms underlying ETT are extinguished or lost in the absence of chemical odors associated with the estuary (i.e., in shelf waters beyond the estuarine plume). Finally, photoresponses of zoeae were characterized in offshore and estuarine waters to determine if their response to light influences their depth distribution and swimming behavior in estuarine and coastal/shelf areas.
Materials and methods Collection of ovigerous crabs and recording of larval activity Ovigerous blue crabs (C. sapidus) and fiddler crabs (U. pugilator) were collected from the Newport River
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Estuary (Beaufort, NC, USA: 3443¢N; 7640¢W; 1 km from the ocean inlet) from June to August 2002. Tides in the area are semidiurnal with a period of 12.4 h and amplitude of 1 m. Berried female blue crabs were collected using dip nets while they were migrating near the surface during nocturnal ebb tides (Tankersley et al. 1998), while ovigerous U. pugilator were collected by hand from their burrows in the upper littoral zone of sandy beaches. Immediately following collection, the developmental stage of the embryos of the egg masses was determined using the procedures of De Vries et al. (1983) and Brown and Loveland (1985). Only crabs that possessed eggs that were determined to be within 24 h of hatching (i.e., late-stage embryos) were used in experiments. Adult blue crabs with late-stage eggs were maintained in the laboratory in individual 23 cm diameter · 14 cm circular glass aquaria containing 2 l of filtered (