Endogenous rhythms and entrainment cues of larval activity in the horseshoe crab Limulus polyphemus

The American horseshoe crab, Limulus polyphemus (Linnaeus), typically inhabits estuaries and coastal areas with pronounced semi-diurnal and diurnal tides that are used to synchronize the timing of spawning, larval hatching, and emergence. Horseshoe crabs spawn in the intertidal zone of sandy beaches and larval emergence occurs when the larvae exit the sediments and enter the plankton. However, L. polyphemus populations also occur in areas that lack significant tidal changes and associated synchronization cues. Endogenous activity rhythms that match predictable environmental cycles may enable larval horseshoe crabs to time swimming activity to prevent stranding on the beach. To determine if L. polyphemus larvae possess a circatidal rhythm in vertical swimming, larvae collected from beach nests and the plankton were placed under constant conditions and their activity monitored for 72 h. Time-series analyses of the activity records revealed a circatidal rhythm with a free-running period of ≈ 12.5 h. Maximum swimming activity consistently occurred during the time of expected falling tides, which may serve to reduce the chance of larvae being stranded on the beach and aid in seaward transport by ebb currents (i.e., ebb-tide transport). To determine if agitation serves as the entrainment cue, larvae were shaken on a 12.4 h cycle to simulate conditions during high tide in areas with semi-diurnal tides. When placed under constant conditions, larval swimming increased near the expected times of agitation. Thus, endogenous rhythms of swimming activity of L. polyphemus larvae in both tidal and nontidal systems may help synchronize swimming activity with periods of high water and inundation.     

Factors affecting the circatidal rhythm in vertical swimming of ovigerous blue crabs, Callinectes sapidus, involved in the spawning migration

Ovigerous blue crabs, Callinectes sapidus, are observed to undergo nocturnal ebb-tide transport (ETT) during their seaward spawning migration. A previous study found that females undergoing the spawning migration have a circatidal rhythm in vertical swimming, which serves as the biological basis for ETT. The present study asked three questions about this endogenous rhythm. First, does the rhythm occur in females with mature embryos regardless of whether they are undergoing ETT? Second, when exposed to a light/dark cycle in the laboratory, do ovigerous females only swim vertically at the time of ebb tide during the dark phase? Third, do attachments to the backs of ovigerous crabs affect the circatidal rhythm? The circatidal rhythm occurred in all crabs with mid-stage embryos that were prevented from undergoing ETT. The rhythm was unaffected by the light/dark cycle, which implies that migration can occur at lower light levels at depth during the day. Finally, attachments did not affect the rhythm, which suggests that tags and transmitters will not affect the spawning migration.     

Comparison of low salinity tolerance in Callinectes sapidus Rathbun and Callinectes similis Williams postlarvae upon entry into an estuary

Planktonic larvae of estuarine crabs are commonly exported to the continental shelf for development and then return to coastal and estuarine areas as postlarvae (megalopae). Megalopae returning to estuaries must be adapted to survive in brackish water whereas those of coastally distributed species should not need such adaptations. We investigated 1) whether megalopae of the estuarine crab Callinectes sapidus and the coastal crab Callinectes similis undergo changes in salinity tolerance upon entry into an estuary and 2) what factors induce those changes. Megalopae were collected at a coastal site and a nearby estuarine site and exposed to a range of salinities (5, 10, 15, 20 and 30) for 6 h. Percent survival was determined after 24 h reintroduction to the collection site water. We also investigated 1) whether increased salinity tolerance was induced by reduced salinity or estuarine chemical cues, 2) the time to acclimation and 3) the salinity necessary for acclimation. C. sapidus megalopae from the estuarine site were more likely to survive exposure to low salinities than those from the coastal site. C. sapidus megalopae from the coastal site exhibited increased survival after acclimation to salinities of 27 and 23 for 12 h. Estuarine chemical cues had no effect on salinity tolerance. C. similis megalopae were less likely to survive at low salinities and did not exhibit an acclimation response upon exposure to reduced salinities. These results suggest that megalopae of C. sapidus are physiologically adapted to recruit to estuaries whereas megalopae of C. similis are unable to acclimate to low salinity conditions.     

Limited gene flow in Uca minax (LeConte 1855) along a tidally influenced river system

For crab larvae, swimming behaviors coupled with the movement of tides suggests that larvae can normally move upstream within estuaries by avoiding ebb tides and actively swimming during flood tides (i.e., flood-tide transport [FTT]). Recently, a 1-D transport model incorporating larval behavior predicted that opposing forces of river discharge and tidal amplitude in the Pee Dee River/Winyah Bay system of South Carolina, USA, could limit dispersal within a single estuary for downstream transport as well as become a dispersal barrier to recruitment of late stage larvae to the freshwater adult habitats of Uca minax (LeConte 1855). We sequenced 394-bp of the mitochondrial cytochrome apoenzyme b for 226 adult U. minax, from four locales along a 49-km stretch of the Pee Dee River/Winyah Bay estuary, above and below the boundary of salt intrusion. Results of an analysis of molecular variance (AMOVA) and an exact test of population differentiation showed a small, but statistically significant (α=0.05) population subdivision among adults of the 4 subpopulations, as well as all subpopulations being significantly differentiated (α=0.05). This pattern fitted with model predictions, which implies that larval transport within the tidally influenced river system is limited.     

Sensory physiology and behavior of blue crab (Callinectes sapidus) postlarvae during horizontaltransport

Adult blue crabs (Callinectes sapidus) live in estuaries and release larvae near the entrances to estuaries. Larvae are then transported offshore to continental shelf areas where they undergo development. Postlarvae, or megalopae, remain near the surface and undergo reverse diel vertical migration. The behaviors underlying this migration pattern are responses to light and a solar day rhythm in activity, in which megalopae are active during the day and inactive at night. Onshore transport probably occurs by wind‐generated surface currents. Once in the vicinity of an estuary, megalopae move up the estuary by selective tidal stream transport, in which they swim in the water column on rising tides at night and are on or near the bottom at all other times. Light inhibits swimming during the day. The ascent into the water column on nocturnal rising tides does not result from a biological rhythm in activity, but rather is cued by the rate of increase in salinity during rising tides. Megalopae have separatebehavioural responses in coastal/shelf areas and in estuaries, which are induced by chemical cues in offshore and estuarine waters.     

Endogenous swimming rhythms underlying secondary dispersal of early juvenile blue crabs, Callinectes sapidus

Blue crab, Callinectes sapidus Rathbun, megalopae settle in seagrass or other complex submerged aquatic habitats in estuaries, where they metamorphose to the first juvenile (J1) crab stage. Within tidal areas, early juveniles (J1-2) leave such nursery areas by undergoing secondary dispersal during nocturnal flood tides. The present study determined whether J1-2 blue crabs have a biological rhythm in vertical swimming activity that contributes to secondary dispersal. Endogenous rhythms in vertical swimming were determined for (1) J1-2 crabs collected from two estuaries with semi-diurnal tides, (2) J1 crabs that metamorphosed from the megalopal stage in the laboratory the day after collection, and (3) premolt megalopae that metamorphosed to J1 crabs under constant conditions during the experiment. In all cases, a circadian rhythm was present in which crabs swam vertically during the time of night in the field. The time of peak vertical swimming did not correspond to the time of flood tide at the collection sites, but did consistently occur at night, with a mean around midnight. While responses to environmental factors probably control the onset and end of vertical swimming by early juvenile blue crabs during flood tides in tidal areas, a circadian rhythm underlies secondary dispersal at night.     

Entrainment of the activity rhythm of the mole crab Emerita talpoida

The mole crab Emerita talpoida migrates with the tide in the swash zone of sand beaches. A circatidal rhythm in vertical swimming underlies movement, in which mature male crabs show peak swimming activity 1-2 h after the time of high tides at the collection site. In addition, there is a secondary rhythm in activity amplitude, in which crabs are maximally active following low amplitude high tides and minimally active following high amplitude high tides. The present study determined the phase response relationship for entrainment of the circatidal rhythm with mechanical agitation and whether the cycle in activity related to tidal amplitude could be entrained by a cycle in the duration of mechanical agitation at the times of consecutive high tides. After entrainment with mechanical agitation on an orbital shaker, activity of individual crabs was monitored in constant conditions with a video system and quantified as the number of ascents from the sand each 0.5 h. Mechanical agitation at the times of high tide, mid-ebb and low tide reset the timing of the circatidal rhythm according to the timing relationship to high tide. However, mechanical agitation during flood tide had no entrainment effect. In addition, a cycle in duration of mechanical agitation entrained the rhythm in activity amplitude associated with tidal amplitude. Both rhythms and entrainment effectiveness over the tidal cycle may function to reduce the likelihood of stranding above the swash zone.     

Vertical movement of mud crab megalopae (Scylla serrata) in response to light: Doing it differently down under

Selective tidal-streaming is a model frequently used to explain how planktonic larvae invade estuaries. The ability of larvae to move vertically in the water column to selectively ride favourable currents and maintain ground gained is critical to this process. The mud crab (Scylla serrata) is a widely distributed, commercially and recreationally important portunid crab but little is known about its estuarine recruitment mechanisms or the vertical migration behaviour of its megalopae. In studies of the blue crab (Callinectes sapidus), important factors identified in the recruitment mechanism include altered vertical swimming behaviours in estuarine and offshore water and an endogenous circadian rhythm. Using laboratory experiments we examined the vertical displacement response of mud crab megalopae to illumination in estuarine and offshore water during the day and the night. Mud crab megalopae released into 1 m high towers swam higher when illuminated than when in darkness. This behaviour was repeated during the day and the night and in offshore and estuarine water. Given the apparent indifference to water type and the fact that mud crab megalopae are rarely caught in estuaries, we propose the model that these crabs do not invade estuaries as megalopae, but settle and metamorphose into small crabs on the coastal shelf before moving along the sea bed into estuarine habitats.     

Rafting on wrack as a mode of dispersal for plants in coastal marshes

Here, I examine the potential for dead plant material, or wrack, to act as a vector of dispersal for plants among coastal marshes along the Palmer River in New England, USA. Three hundred mats of wrack floating along a 2.5 km section of river spanning tidal fresh, brackish and salt marshes were sampled for propagules of plants from May 1997 to October 1998. Thirty species of plants and 2 species of algae were associated with the wrack, and 24 of the plant species were viable under greenhouse conditions. Common and abundant species of tidal fresh, brackish and salt marshes were found in the wrack, as well as introduced and invasive species. Wrack contained plants suited to different modes of dispersal, including water, wind and adherence to animals. Measurements of the movement of individual mats of wrack along a 200 m section of the river indicated that wrack travelled at speeds ranging from 1.1 to 2.6 km h⁻¹, which translates to potential dispersal distances ranging from 6.5 to 15.9 km for one ebb or flood tide of 6 h duration. Tagged mats of wrack tracked for one ebb or flood tide travelled at least 2.5 km along the river. These results suggest that wrack may be an important agent of plant dispersal among coastal marshes in estuaries.     

Time-keeping system of the eel pout, Zoarces viviparus

Observations on the rhythmic activity of 71 juvenile specimens of the inter-tidal blenny Zoarces viviparus reveal an endogenous pattern of swimming at three different periodicities. Circatidal swimming, with activity peaks phased to high water or the ebb of the subjective 12.4-h tides, was found in 50 fish and was the predominant pattern seen immediately after collection, when the rhythm generally persisted for between 3 and 12 cycles. Discrete activity peaks, with a free running period of approximately 24 h were also evident in the swimming pattern of eight fish. A circadian influence was also manifest as a modulation in amplitude, phase shifts and changes in free-running period of the circa-tidal rhythm. Overall, the activity level declined with time but those fish that remained active long enough showed a semi-lunar rhythm, with maximum activity at the time of the spring tides. A comparison of the behavior of animals collected at different times of the year suggests a seasonal variation in the persistence of circatidal swimming. The results are consistent with a control system involving circatidal, circadian, and semi-lunar oscillators. (Chronobiology International, 18(1), 27-46, 2001)     

Rhythms of Locomotion and Oxygen Consumption in the Estuarine Amphipod Corophium Volutator (Crustacea: Amphipoda)

The estuarine amphipod Corophium volutator exhibits an endogenous circatidal rhythm of swimming activity, with maxima occurring just after the expected time of high water, under constant laboratory conditions. Oxygen uptake by Corophium is also subject to modulation across the tidal cycle. The period of highest oxygen uptake occurs during the ebb tide, in phase with the period of maximum swimming activity. A second increase in oxygen uptake during the early flood tide is thought to reflect either in-burrow activity or a previously described rhythm of emergence. This being so, this aspect of the animal's respiratory metabolism may be regulated by an autonomous oscillator independent of that governing the animal's swimming behaviour.     

Behavioural basis of intertidal zonation in Eurydice pulchra Leach

Eurydice pulchra Leach freshly collected at neap and spring tides exhibits an endogenous circatidal rhythm of swimming when kept without sand in constant conditions in laboratory aquaria. When provided with sand in the laboratory, tidally-phased swimming may occur spontaneously at some times of the lunar month, predominantly after the times of highest spring tides but not at neaps. In these cases, therefore, there appears to be clearly demonstrated for the first time in a marine animal a circasemilunar pattern of emergence from the substratum which is coupled to a circatidal rhythm of swimming; the isopods in the laboratory emerge from the sediment only when the swimming rhythm and emergence rhythm are at their maxima. In the field at neap tides some isopods emerge to swim at high tide, dependent upon their responses to water agitation, their feeding state and responses to light. At and just after spring tides in the field large numbers of the isopods swim at high tide, triggered by the endogenous circasemilunar rhythm of emergence which in the field is probably cued by the effects of increased water agitation. The main function of the endogenous circatidal rhythm of swimming appears to be to permit the isopods to return to their preferred zone in the sand before the fall of the tide. The coupled circasemilunar rhythm of emergence which induces greater swimming at spring tides reduces the risk of animals being stranded high on the shore during neap tides.     

Feeding by fish visiting inundated subtropical saltmarsh

Australian saltmarshes are inundated less frequently and for shorter periods than most northern hemisphere marshes, and when inundated provide transient fish a diverse prey assemblage. We determined the extent of feeding on saltmarsh by examining stomach contents of a common marsh transient, glassfish (Ambassis jacksoniensis), in the Coombabah estuary in subtropical Queensland. We tested the hypotheses that fish caught after visiting the marsh (after (M)) would have similar quantities of food (stomach fullness index, SFI) but different prey composition (abundance, weight) both to fish collected before (Before) saltmarsh inundation and to fish that had not visited the marsh but were caught after marsh inundation (After (NM)). Sampling was done on multiple nights over 3 months in winter, when the marsh is inundated on spring tides at night only. SFI values of After (M) fish were significantly higher (SFI ≈ 12%) than those of Before and After (NM) fish (SFI ≈ 0-1%). After (M) fish also had very different prey composition, eating more crab zoea (> 100 zoea fish^− 1) than Before fish (10) and After (NM) fish (0). After (M) fish showed a consistent pattern in zoea abundances among sampling nights, in all months, with lower zoea abundances on the first night that the marsh was inundated than on subsequent nights. This is attributed to the synchronized spawning of crabs resident on the marsh, releasing their zoea on the ebb of the second inundating tide of the month. Fish stomach contents did not differ before and after smaller high tides not inundating the marsh (SFI ≈ 0-1%). Experimental evidence showed that glassfish evacuate their stomach contents in about an hour under starvation conditions, further strengthening our contention that the stomach contents of After (M) fish represent prey ingested on the marsh. The demonstration of intensive feeding by fish visiting this marsh points to a potentially important role of saltmarsh in the trophodynamics of subtropical Australian estuaries.     

Morphological and behavioral antipredatory adaptations of decapod zoeae

Summary Zoeae of some species of estuarine decapods are retained in the estuary throughout development while others are exported into nearshore coastal waters. The horizontal migrations of decapod zoeae to coastal waters may have evolved to reduce the probability of encountering planktivorous fishes which are most abundant in the estuary. If so, then the morphological vulnerability of zoeae to fish predation should be inversely related to the number of predators occurring where they develop. Six species of estuarine decapod zoeae were offered to Menidia menidia and Fundulus heteroclitus. The behavioral interactions were observed to determine the prey's vulnerability to predation, and the mode of operation and relative effectiveness of their defenses. Feeding trials and behavioral observations both demonstrated that M. menidia 6–16 mm long preferred Uca minax and Callinectes sapidus zoeae, which are exported from the estuary, to Rhithropanopeus harrisii, Sesarma reticulatum and Palaemonetes pugio, which are retained within estuaries. Pinnotheres ostreum zoeae develop in the lower estuary and fish demonstrated an intermediate preference for the zoeae. Menidia menidia 20–40 mm long showed similar preferences for R. harrisii S. reticulatum, P. ostreum and U. minax as did small silversides. Large-mouthed demersal fish, Fundulus heteroclitus 6–10 mm long, also preferred U. minax to R. harrisii, but more readily preyed on zoeae than did M. menidia. The exported species of zoeae have shorter spines and smaller bodies than do retained zoeae, except P. ostreum which is small, spineless and passively sinks when attacked by fish. Other retained species of zoeae also have postcontact behavioral defenses which enhance the effectiveness of their morphological defenses. Zoeae do not evade attacks by fishes, but fishes quickly learned to avoid zoeae, which increases the effectiveness of the zoeae's antipredatory adaptations.     

Circatidal rhythmic behaviour in the coastal tiger beetle Callytron inspecularis in Japan

Larvae of the coastal tiger beetle Callytron inspecularis (W. Horn) (Coleoptera: Cicindelidae) plug their burrow opening before submergence at high tide. Field observations showed that burrow plugging was a rhythmic behaviour that coincided with the tidal cycle (ca. 12.4 h). On average, larvae plugged their burrows 41.8 min before the tide covered the habitat. The mean interval between consecutive burrow-plugging events in the field was 12.40 h. In the laboratory, in the absence of tidal inundation, the mean interval between consecutive burrow-plugging events was 12.45 h. This suggests that the burrow-plugging rhythm of the coastal tiger beetle is governed by an endogenous circatidal rhythm.     

Swimming activity responses to water current reversal support selective tidal-stream transport hypothesis in juvenile thinlip mullet Liza ramada

Swimming activity of thinlip mullet Liza ramada in response to water current reversal was investigated experimentally. A total of 130 young of the year thinlip mullet ranging in size from 22 to 36 mm were entered in trials with four different conditions over three weeks. The fish were subjected to current reversal (6.2/6.2 h) and a Light-Dark cycle (12/12 h). Swimming direction (with or against the current) was video-recorded throughout the experiments. The mullet showed an effective synchronisation of their swimming activity to water current reversal and Light-Dark cycle. This synchronisation could demonstrate the existence of a diurnal selective tidal-stream transport in the natural environment as observed in the two other European catadromous species.     

An entrainment model for semilunar rhythmic swimming behaviour in the marine isopod Eurydice pulchra Leach

Entrainment experiments have been carried out with geographically widely separated populations of the sand beach isopod Eurydice pulchra Leach subjected to periods of simulated tidal agitation imposed concurrently with a 24-h light: dark (L: D) cycle. Circatidal swimming rhythms of greatest amplitude were induced when agitation was applied with the subjective timing, within the L: D cycle, of local spring high tides. This occurred in a normal L: D regime and also when the L: D regime was phase shifted through 90°. Animals previously maintained in constant darkness (D: D) and subsequently exposed to simulated tidal disturbance at various times in constant darkness were unable to modulate the amplitude of circatidal swimming activity. Isopods previously maintained in a normal L: D cycle and subsequently subjected to artificial tidal agitation in constant darkness were, however, able to modulate circatidal activity. This indicates that E. pulchra is capable of detecting tidal agitation and daily light cues and using them in conjunction with its circadian “clock” to modulate its endogenous circatidal rhythmicity. The free-running semilunar rhythm of swimming activity entrained only when the timing of agitation within the day/night cycle mimicked the pattern of local spring high tides. Agitation with the timing of neap high tides entrained no free-running circa-semilunar activity pattern.     

Hatching rhythms and dispersion of decapod crustacean larvae in a brackish coastal lagoon in Argentina

Mar Chiquita, a brackish coastal lagoon in central Argentina, is inhabited by dense populations of two intertidal grapsid crab species,Cyrtograpsus angulatus andChasmagnathus granulata. During a preliminary one-year study and a subsequent intensive sampling programme (November–December 1992), the physical properties and the occurrence of decapod crustacean larvae in the surface water of the lagoon were investigated. The lagoon is characterized by highly variable physical conditions, with oligohaline waters frequently predominating over extended periods. The adjacent coastal waters show a complex pattern of semidiurnal tides that often do not influence the lagoon, due to the existence of a sandbar across its entrance. Besides frequently occurring larvae (exclusively freshly hatched zoeae and a few megalopae) of the two dominating crab species, those of three other brachyurans (Plathyxanthus crenulatus, Uca uruguayensis, Pinnixa patagonica) and of one anomuran (the porcellanidPachycheles haigae) were also found occasionally. Caridean shrimp (Palaemonetes argentinus) larvae occurred in a moderate number of samples, with a maximum density of 800·m⁻³. The highest larval abundance was recorded inC. angulatus, with almost 8000°m⁻³. Significantly moreC. angulatus andC. granulata zoeae occurred at night than during daylight conditions, and more larvae (statistically significant only in the former species) during ebb (outflowing) than during flood (inflowing) tides. In consequence, most crab zoeae were observed during nocturnal ebb, the least with diurnal flood tides. Our data suggest that crab larvae do not develop in the lagoon, where the adult populations live, but exhibit an export strategy, probably based upon exogenously coordinated egg hatching rhythms. Zoeal development must take place in coastal marine waters, from where the megalopa eventually returns for settlement and metamorphosis in the lagoon. Significantly higher larval frequency ofC. granulata in low salinities (≤12‰) and at a particular sampling site may be related to local distribution patterns of the reproducing adult population. Unlike crab larvae, those of shrimp (P. argentinus) are retained inside the lagoon, where they develop from hatching through metamorphosis. They significantly prefer low salinity and occur at the lagoon surface more often at night. These patterns cannot be explained by larval release rhythms like those in brachyuran crabs, but may reflect diel vertical migrations to the bottom. It is concluded that osmotic stress as well as predation pressure exerted by visually directed predators (small species or life-cycle stages of estuarine fishes) may be the principal selection factors for the evolution of hatching and migration rhythms in decapod larvae, and that these are characteristics of export or retention mechanisms, respectively.     

Growth rates of baldcypress (Taxodium distichum) seedlings in a treated effluent assimilation marsh

Wetlands have proven effective at improving water quality of treated wastewater effluent, which in turn promotes increased primary productivity and vertical accretion. Baldcypress (Taxodium distichum) seedlings grown under different conditions (bare root and potted) were planted in four subunits of an effluent assimilation marsh and a control marsh in southeast Louisiana, USA, and basal diameter growth was monitored over one growing season. Mean basal diameter growth for seedlings in the assimilation subunits ranged from 16.1 (±1.4) mm to 9.5 (±0.9) mm, whereas growth for seedlings planted in the control marsh was 6.4 (±0.9) mm. Seedlings planted nearest the outfall experienced greater basal diameter growth (18.1 ± 2.6) compared to those planted 700 m away (8.0 ± 0.9), with growth generally decreasing with distance. Potted seedlings experienced greater growth (19.1 ± 1.0 and 20.6 ± 1.0 for five-month-olds and ten-month olds, respectively) than bare root seedlings (4.6 ± 0.6 and 4.0 ± 0.4 for one-year-olds and two-year olds, respectively). Planting assimilation marshes with baldcypress seedlings can be an effective restoration tool for coastal Louisiana, which will provide hurricane protection and improved surface water quality. Wastewater treatment wetlands may offer an effective tool for restoring coastal baldcypress (T. distichum)-water tupelo (Nyssa aquatic) swamps in Louisiana.     

A comparison of the activity patterns of the sand goby Pomatoschistus minutus (Pallas) from areas of different tidal range

Sand gobies ( Pomatoschistus minutus ) collected from beaches with a large tidal range (Scotland) exhibit a circatidal rhythm of activity in constant conditions in the laboratory. There is no endogenous circadian component to the rhythm. The phasing of the rhythm is such that peak activity occurs at the predicted time of ebb tide. Light-dark (LD) cycles applied in the laboratory have a marked effect on activity greatly enhancing it at night so that the original tidal rhythm becomes nocturnal. Some evidence was obtained that LD cycles can entrain a weak nocturnal circadian rhythm in fish removed from tidal conditions. Contrary to expectations, some fish from beaches with a small and unpredictable tidal range (Oslofjord, Norway) also show a weakly persistent circatidal thythm without an endogenous circadian component, but great variability was noticed between individual fish. Laboratory LD cycles did not entrain a persistent circadian rhythm in the fish from the Oslofjord.