Plasticity in the temporal organization of behaviour in the limpet <Emphasis Type="Italic">Cellana grata</Emphasis>

The behaviour of intertidal consumers is often tightly constrained to tidal movements, although activity patterns can vary within these constraints. Spatio-temporal variability in behaviour of a limpet, Cellana grata, was analysed over different tidal conditions (spring and neap tides) and during different times of the year (one summer and one winter) at sites in Hong Kong. Activity was generally dictated by tidal movements, being concentrated when animals were awash. Plasticity in behaviour was observed, with some limpets anticipating activity during the summer period and delaying activity during winter time. Limpets were active for a time equal, or slightly less, than time awash. As the time awash exceeded ~14–16 h, however, activity duration decreased. Within this general pattern, tidal variation as well as variation among times of the year was noted, with the lowest dependence on time awash being recorded during winter neap tides. Limpets showed a slight preference for being active during nighttime, which was particularly evident when animals were emersed during the summer period. Although the basic activity in C. grata is constrained to a specific temporal window, this limpet is able to modulate its foraging strategies and resting height, according to local, daily changes in environmental conditions.     

Foraging and homing behaviour in the high-shore, crevice-dwelling limpet Helcion pectunculus (Prosobranchia: Patellidae)

The foraging activity of the high-shore, crevice-dwelling limpet Helcion pectunculus (Gmelin, 1791) (Prosobranchia: Patellidae) from an exposed shore on the eastern Cape coast of South Africa was monitored. Activity was compared during spring and neap tides and between spring, summer, autumn and winter. Rhythms of activity in this limpet varied depending upon microhabitat; individuals inhabiting both east- and west-facing rock surfaces were active during nocturnal low tides, but limpets on west-facing rock surfaces were also active during daytime low tides, whilst in the shade. Individuals travelled further during foraging excursions in winter (xˉ=85.53 cm) than in either spring (xˉ=55.7 cm) or summer (xˉ=48.8 cm) and also during spring low tides (xˉ=89.8 cm) compared with neaps (xˉ=40.9 cm). H. pectunculus exhibited rigid homing to a fixed scar within a crevice, and feeding excursions were found to consist of three distinct phases: a relatively rapid outward phase, a much slower foraging phase and a rapid homeward phase. Whether or not these limpets graze throughout an excursion is not known. Foraging was always highly directional, with a mean vector which took limpets onto an area of the rock face with the highest microalgal biomass. The fact that H. pectunculus took advantage of optimal feeding areas and memorized their location to enable return visits suggests a learning component in herbivorous gastropod foraging behaviour. Received: 29 December 1997 / Accepted: 8 May 1998     

Rhythmic vertical migration of the gastropod Cerithidea decollata in a Kenyan mangrove forest

In Mida Creek, Kenya (3°20′S, 40°5′E), at high water, the snail Cerithidea decollata dwells on the trunks of mangrove trees (Avicennia marina), while during low water it migrates to the ground, foraging at various distances from the trunk, where it aggregates again well before the incoming tide. Snails from the upper shore level are 150–200 m distant from those living at the lower shore level and they cluster at lower heights on trunks. In any case, sufficient height is usually attained to avoid being submersed. An experiment was designed (February and October 2005), exchanging individuals from different shore levels subject to different tide regimes, in order to test whether snails rely on internal information or on external, direct cues, to adapt their behaviour to local conditions. Results show that C. decollata mostly rely on internal information, presumably based on an internal clock. When individuals from upper and lower shore levels were exchanged, their internal clocks continued to govern when to ascend the home trunk and how high to climb for five to six successive tides, after which the behaviour was reset to the new local conditions.     

Factors affecting variability of foraging excursions in a population of the limpet Patella vulgata (Mollusca,Gastropoda)

Paths moved by the limpet Patella vulgata L. were monitored on a sheltered vertical rocky shore in North Wales using time-lapse photography throughout nocturnal low tides in April and November 1992, roughly corresponding to periods of minimum and maximum gonad ripeness, respectively. Various motion parameters, including total duration, total length, and maximum distance reached from home were computed from 124 complete foraging routes obtained from 18 higher-zoned and 18 lower-zoned limpets. P. vulgata typically performed a single loop per night (average total length, ca. 70 cm), moving from the individual home scar to graze the surrounding algal grounds (average maximum distance, ca. 25 cm), then following its own trail back home. On the average, limpets moved from the home scar during three of four available nocturnal low tides and exploited about half the emersion time. Evidence for size-related variability in behaviour was found, as a positive correlation was assessed between both total duration and legth of the excursions, and shell length. In addition, zonation was proved to affect the limpets' foraging behaviour, since low-shore limpets moved faster and covered greater distances than high-shore ones. Moreover, consistent seasonal variation in foraging behaviour emerged, since in April the excursions were longer and longer-lasting than in November, but limpets exploited a larger fraction of potential activity phases in November than in April. The within-population variability in the temporal and spatial characteristics of the foraging excursions is discussed in relation to the available data on zonal and seasonal variation of food resources and in relation to physiological changes due to reproductive cycle.     

Circatidal rhythm of an intertidal crab, Hemigrapsus sanguineus : synchrony with unequal tide height and involvement of a light-response mechanism

The circatidal rhythm of intertidal animals may reflect the inequality of the tides. In addition, a light-sensitive mechanism may be involved in their internal timing systems. To test these hypotheses, the larval release activity of the intertidal crab Hemigrapsus sanguineus was monitored under different light conditions in the laboratory. Under a 24-h light–dark (LD) cycle with the phase similar to the field, the activity coincided with the times of high tide in the field and showed a tidal rhythm. This rhythm free-ran in constant, dim-light conditions, suggesting that the timing is controlled by an endogenous clock. When the population was exposed to a 24-h LD cycle with the phase changed from that in the field, the tidal rhythm was phase-shifted; while the light cycle advanced in phase from the field caused a phase-advance of the rhythm, that delayed in phase induced a phase-delay of the rhythm. Thus, a light-response mechanism is definitely involved in circatidal timing systems. But the population rhythm showed a large variability among individuals, associated with the phase-shift, and the magnitude of the phase-shift did not accurately correspond to that of the light cycle. These results suggest that the light-response system can control the phase of the rhythm less stronger than that in estuarine crabs. Most releases occurred at higher high tides, but the release of some females obviously occurred at lower high tides. The larval release pattern thus could not be accounted for by a simple synchrony with higher high tides. Hatching of H. sanguineus occurred after a “hatching program” of 49.5 to 52.5 h. This program is initiated by some factor (hatching-program inducing stumuli: HPIS) transmitted from the female to the embryos. We speculated that this factor is effectively transmitted to the embryos when the habitat is exposed to air, i.e., at lower low-tide periods, and that once each embryo is stimulated, hatching occurs synchronously 2 d later during high tide. The release of HPIS is probably controlled by the circatidal clock of the female, and the 24-h LD cycle may participate in shifting this timing to the opposite low tide. Received: 14 January 1997 / Accepted: 18 February 1997     

Substratum relationships of some tropical Pacific intertidal gastropods

Among tropical Indo-West Pacific herbivorous intertidal gastropods, high intertidal neritids, and limpets and certain lower intertidal limpets are restricted to a narrow range of substratum types. Littorinids, planaxids, low intertidal neritids, most lower intertidal limpets, and the trochid Monodonta labio tolerate a wide variety of substrata. This pattern of substratum specialization is related to the overall adaptive strategies of the various groups: those with a large area of soft tissue in contact with the substratum (neritids and limpets) often specialize to a particular substratum, especially at high shore levels, while those in which the area of contact between animal and substratum is small do not. High intertidal neritids and limpets able to live on a wide range of substrata tend to be species of limited geographic distribution. It is concluded that, even within a tropically similar group of animals (raspers in this case) relevant dimensions of niche separation depend upon the structure of the environment as well as upon the structure of the animals themselves.     

Life-history features of the marine intertidal limpet Notoacmea scutum (Gastropoda) in central California

Growth of individually marked specimens of Notoacmea scutum (Rathke) was followed for 15 months (April, 1978 to June, 1979) at a field site in central California, USA. Growth rates were highly seasonal, being highest from late spring through early summer and lowest during winter. Growth rate also varied significantly with intertidal height: limpets lower in the intertidal zone grew faster. Both relationships may have been related to the relative abundance of food or to the amount of time available for foraging. Recently settled limpets, which were present throughout the year, grew to approximately 17 mm in length by the end of their first year; by then, they had also reached the size at which mature gonads were consistently found (16 mm). Limpets were almost 26 mm long by the end of the second year. Substantial mortality occurred throughout the year, but it was particularly severe during winter, when a large portion of the reproductive population was lost. This pronounced winter mortality was probably not caused by invertebrate predators such as seastars. Most limpets at the study site were less than 2 yr old.     

Gezeitenrhythmische Nahrungsaufnahme und Kotballenablage einer terrestrischen Milbe (Oribatei: Ameronothridae) im marinen Felslitoral

Feeding, locomotory and defecatory activity of the algivorous orbatid mite Ameronothrus marinus have been measured under defined conditions in the laboratory. Of terrestrial origin, these mites inhabit the intertidal zone of rocky shores along the North and Baltic Seas. Under daylight cycles found at the sampling site and in the absence of tides, feeding and defecation follow an endogenous rhythm with a spontaneous period of 12.3 h; in the tideless littoral of the Baltic Sea these activities are synchronized with diurnal cycles. Feeding and defecation follow a definite sequential pattern, repeated on the average every 4 h, i.e., 3 times between two high tides. The phase of this tidal feeding-defecation rhythm is determined by the onset of the high tide, and different patterns of this rhythm can be observed according to the tidal zones. Inhabitants of the lower eulittoral exposed to longer periods of submersion start feeding earlier, take up more food at one time before the beginning of high tide, quickly defecate part of the food undigested after feeding, and later produce other faecal pellets which contain the real remains of digestion. Inhabitants of the upper eulittoral, exposed to shorter periods of submersion, start feeding later and extend their feeding activity over the whole period of low tide; the difference between faecal pellets with digested and undigested contents is indistinct. The occurrence of these different types of faecal pellets in inhabitants of the intertidal zone is interpreted as a compensatory physiological adaptation resulting from increasing periods of submersion.     

Intra-specific variability in the temporal organisation of foraging activity in the limpet<Emphasis Type="Italic"> Patella vulgata</Emphasis>

Patella vulgata is one of the most common limpet species on rocky shores throughout the north-eastern Atlantic. Foraging activity of this species has been described during various different diel and tidal phases and several factors have been suggested that might influence the timing of its activity. Among these, inclination of rock surfaces seems to have a clear role, with limpets on horizontal rocks being active during daylight at high water, while limpets on vertical rocks were active during night-time low water. However, by comparing the results of previous investigations it is difficult to separate clearly the effect of any single factor from the effects of their interactions. In the present paper we investigated the simultaneous influence of height on the shore, slope of rock surface and date of sampling (August–September and March–April) on the behaviour of a population of P. vulgata on the Isle of Man (UK). The study was carried out using modern telemetric methods, allowing the activity patterns of limpets to be recorded for long periods of time. The results showed that limpets concentrated their activity during two distinct temporal windows—daytime tide-in and night-time tide-out—while no significant activity was observed during daytime tide-out or night-time tide-in. The observed behaviour appeared to be driven by complex interactions among the three factors examined, and the influence of rock slope alone was not so strong as to override the effect of other factors completely. In addition, a key finding of this study was the conspicuous variability in the individual behaviour of P. vulgata. The greatest level of variability was observed in limpets on vertical surfaces on the upper shore, which showed an extreme switch in behavioural patterns, according to date of sampling (daylight/tide-in foraging during the spring and night-time/tide-out foraging during late summer). In addition, individuals apparently sharing the same set of conditions (inclination, height on the shore and sampling date) differed in their behaviour, and a given behavioural pattern was not always shared by all individuals from a given group. Finally, variability was also observed at the intra-individual level since the same individual could be active during different tidal and diel phases. In conclusion, although the existence of endogenous rhythms has previously been demonstrated in this species, our data clearly show that P. vulgata was able to modulate its behavioural patterns in relation to a variety of exogenous determinants.Communicated by R. Cattaneo-Vietti, Genova     

How hot for how long? The potential role of heat intensity and duration in moderating the beneficial effects of an ecosystem engineer on rocky shores

Studies of the importance of ecosystem engineers have focused on their benefit to biodiversity through ameliorating environmental stress, without understanding the exact benefits gained by associated organisms. On monsoonal tropical shores, species experience strong seasonality in environmental conditions from almost temperate winters to tropical summers when mass mortalities can occur during daytime emersion. The limpet, Cellana grata, associates with an ecosystem engineer, the barnacle Tetraclita japonica, in summer, but not in winter. To understand the benefits of this association, physiological responses (heart rates and osmotic responses) of the limpet either amongst Tetraclita or on open rock surfaces were investigated under three environmental conditions in a laboratory mesocosm: awash (non-stressed), low (30 °C) and high thermal stress (40 °C) of varying durations (3 or 6 h). In general, at 30 °C, limpets showed similar physiological responses under all conditions for both exposure durations. After 6 h at 40 °C, however, all limpets on open rock surfaces died, whereas those associated with barnacles survived. The surviving limpets experienced similar levels of stress as those exposed to 40 °C on open rock surfaces for half the time (3 h), showing that both the level and duration of stress were important. Limpets, therefore, gain benefits from engineering species when conditions are extreme or stress is prolonged. Under low temperatures or for short durations (e.g. winter), associating with barnacles does not provide physiological benefits. Understanding how, and to what extent, associates benefit from ecosystem engineers highlights how close the margin between survival and mortality can be when conditions are extreme.     

Field observations on the rhythmic behaviour of Nerita textilis (Gastropoda: Prosobranchia)

Field observations on Nerita textilis Dillwyn inhabiting rocky cliffs at Sar Uanle (Southern Somalia) revealed that during the resting phase some of the snails are scattered on the upper cliff and some are clustered at lower levels. During feeding they all migrate downward, but to different extents. Maximum activity of both groups occurs during low water (LW) between midday and midnight. During spring tides (ST), the scattered snails reside higher up and make smaller feeding excursions than during neap tides (NT). During ST, some clustered snails join the belt of scattered individuals, while the trend reverses during NT. A diurnal and a tidal component appear in their periodicity.Publication of the Centro di Studio per la Faunistica ed Ecologia Tropicali del C.N.R. Researches on the coast of Somalia. The shore and the dune of Sar Uanle, No. 14.     

Morphological patterns in high-intertidal gastropods: Adaptive strategies and their limitations

An analysis of shell form in several families of high-intertidal herbivorous gastropods has revealed the existence of morphological gradients. Among tropical littorinids, relative spire height and degree of development of external shell sculpture generally increase interspecifically, and often intraspecifically, from low to high shore levels. This gradient is also evident from temperate to tropical latitudes, and may be modified or overridden by exposure to wave action and other factors. Among acmaeid, patellid, and siphonariid limpets, there is a well-marked interspecific increase in relative shell height with increasing shore level, but latitudinal trends in morphology cannot at present be distinguished. Evidence from both tropical and temperate coasts indicates that limpets found in shaded places tend to have smoother shells than those often exposed to direct sunlight. In the Neritidae, relative shell globosity tends to increase interspecifically from low to high shore levels; most high-shore species have strong shell sculpture, with the base of the shell only slightly excavated. A decrease in the number of neritid species towards higher latitudes is accompanied by selective deletion of globose, strongly sculptured types living at high shore levels. Neritids and some limpets can employ evaporative cooling as a mechanism for temperature regulation. The morphological gradients in these groups reflect a relative increase in the volume of the extravisceral cavity (water reservoir) and a decrease in the area in contact with the substratum, as well as a relative decrease in the rate of water loss, in an upshore direction. Neritids are better adapted than limpets to high temperature and desiccation stresses because of their ability to regulate rate of evaporation and contact between soft parts and substratum. These differences are reflected in the complementary patterns of latitudinal diversity in the two groups. In Littorinidae, which attach to the substratum by a mucus film, the morphological gradients reflect a minimization of water loss and substratum contaet, and a maximization of reflective relative to absorptive surface area.This paper is an expanded version of part of a Ph. D. dissertation presented to Yale University.     

Assessment of factors affecting heart rate of the limpet Patella vulgata on the natural shore

 Heart rate variations of a population of the limpet Patella vulgata were monitored in the natural environment (Lough Hyne, southern Ireland) by non-invasive, optoelectronic recording. The heart rates of 145 limpets of different sizes, living on vertical and horizontal substrata, were measured both in air and water at different environmental temperatures, while the animals were inactive on their home scars. The heart rates of emersed, inactive limpets were positively related to air temperature and negatively related to limpet size. These relationships were similar for limpets on vertical and horizontal substrates. In contrast, no significant relationship between heart rate and temperature was found in submerged limpets, probably due to the narrow thermal range of the water during the study period. During submersion, a significant negative relationship between heart rate and size was evident for limpets on vertical surfaces but not for limpets on horizontal surfaces. In general, submerged limpets had a higher heart rate, 1.16 times that of limpets exposed to air. Moreover, the heart rates of nine animals were recorded while they were moving and while inactive on their home scars. Active limpets had a faster heart rate, 1.6 times that of limpets resting on their home scars. The dependence of heart rate on environmental temperature, size, respiratory medium and activity, as observed in limpets on the shore, agrees well with laboratory data and with previous findings of the correlation of oxygen consumption with the same factors. Such in situ measurements may, therefore, prove useful in attempts to determine natural levels of energy expenditure in models on the behaviour of foraging molluscs. Received: 5 September 1999 / Accepted: 17 April 2000     

Endogenous swimming rhythms underlying the spawning migration of the blue crab, Callinectes sapidus: ontogeny and variation with ambient tidal regime

Spawning female blue crabs, Callinectes sapidus, use ebb-tide transport (ETT) to migrate seaward. In estuaries with semi-diurnal tides, ETT in ovigerous blue crabs is driven by a circatidal rhythm in vertical swimming in which crabs ascend into the water column during ebb tide. The ontogeny of this rhythm was examined by monitoring swimming behavior of females before the pubertal molt, females that had recently undergone the molt but had not yet produced a clutch of eggs, and ovigerous females from an estuary with strong semi-diurnal tides. To assess variation in swimming rhythms with ambient tidal regime, swimming rhythms of ovigerous females from semi-diurnal (Beaufort, North Carolina), diurnal (St. Andrew Bay, Florida), and non-tidal (South River, North Carolina) estuaries were compared. Experiments were conducted during the summers of 2006–2008. Female crabs prior to oviposition had variable endogenous swimming rhythms (circadian, circatidal, or circalunidian). Ovigerous females from estuaries with semi-diurnal and diurnal tides had pronounced circatidal or circalunidian rhythms with swimming during the time of ambient ebb tide. Swimming rhythms of several ovigerous crabs switched between circatidal and circalunidian during the ~5-day observation period. Ovigerous crabs from a non-tidal estuary had a circadian rhythm with vertical swimming around the time of sunset. These results suggest that, while endogenous swimming rhythms are present in some female blue crabs prior to oviposition, rapid seaward movement via ETT in tidal estuaries begins following oviposition of the first clutch of eggs.     

Endogenous control of timing of metamorphosis in megalopae of the shore crab Carcinus maenas

Batches of hundreds of freshly collected megalopae of the shore crab Carcinus maenas (L.) showed persistent circatidal rhythms of moulting to the juvenile crab stage when maintained in constant laboratory conditions. Peaks of moulting occurred around expected times of high tides, with few megalopae moulting at other times. In larvae collected offshore, the highest tidally-timed peak of metamorphosis occurred during the second to fifth expected times of high tide, and metamorphosis of 50% of each batch took about 22 h or longer. In contrast, in larvae collected at the water's edge, 70% metamorphosed during the first expected episode of high tide, within 6 to 8 h after collection. However, although inshore megalopae moulted before offshore ones, the tidal timing of moulting remained unaltered whether megalopae were collected at neaps or springs, from the water's edge or farther offshore, in the presence or absence of natural substratum, and under various light–dark and salinity regimes. Metamorphosis of C. maenas megalopae around the times of high tides may enhance settlement into the upper intertidal zone. Early juveniles of the crab apparently prefer that zone as they are most abundant there and, unlike adults, do not undertake up-and-down-shore migration with tides. The present finding demonstrates, for the first time, endogenous physiological timing of circatidal periodicity in the metamorphic moult of crab megalopae, suggesting that endogenous factors, as well as exogenous ones should be taken into account in considering the process of settlement by crab megalopae. Received: 21 February 1996 / Accepted: 27 November 1996     

Scarred limpets at hydrothermal vents: evidence of predation by deep-sea whelks

The chaotic physical and chemical environment at deep-sea hydrothermal vents has been associated with an ecosystem with few predators, arguably allowing the habitat to provide refuge for vulnerable species. The dominance of endemic limpets with thin, open-coiled shells at north Pacific vents may support this view. To test their vulnerability to predation, the incidence of healed repair scars, which are argued to reflect non-lethal encounters with predators, were examined on the shells of over 5,800 vent limpets of Lepetodrilus fucensis McLean (1988) that were collected from 13 to 18 August 1996. Three vent fields on the Juan de Fuca Ridge at ca. 2,200 m depth were sampled, two within 70 m of 47°56.87′N 129°05.91′W, and one at 47°57.85′N 129°05.15′W with the conspicuous potential limpet predators, the zoarcid fish Pachycara gymninium Anderson and Peden (1988), the galatheid crab Munidopsis alvisca Williams (1988), and the buccinid snail Buccinum thermophilum Harasewych and Kantor (2002). Limpets from the predator-rich vent were most often scarred, a significant difference created by the high incidence of scars on small (<4 mm long) limpets in this sample. Collected with the limpets were small (median shell diameter 4.4 mm) buccinids. They, rather than the larger, more conspicuous mobile fishes and crabs are argued to be the shell-damaging predator. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Rhythmic patterns of abundance in small sublittoral crustaceans: variety in the synchrony with day/night and tidal cycles

Temporal fluctuations of abundance (or emergence) in small benthic and planktonic crustaceans were studied in shallow subtidal waters (1.5 to 3.5 m in tide height). The abundances were more or less rhythmic, and showed wide diversity ranging from very clear nocturnal patterns to patterns in sychrony with the tidal cycle alone. These abundance patterns were classified into categories relating to the degree of synchrony with day/night and tidal cycles. Nocturnal patterns were especially strong in benthic crustaceans, which would be inactive during the daytime, being attached to algae and stones or disappearing into rock crevices, and actively swim in the water at night. Mysis larvae also showed a clear nocturnal pattern. Their lifestyle might be similar to that of many benthic animals. Other planktonic crustaceans drifting in the water showed weak nocturnal patterns. In some planktonic crustaceans (e.g., Calanoida), the ratio of abundance in the surface and bottom samples was reversed between day and night. Their pattern might be a manifestation of weak diel vertical movement between day and night. Furthermore, most patterns of zooplankton and benthos were modified in synchrony with tides to various degrees. Small crustaceans may respond to changes of hydrologic variables fluctuating with the tides, which may exogenously produce a weak tidal component in their emergence patterns. Received: 12 January 1998 / Accepted: 29 August 1998     

Nocturnal feeding migrations of Nerita plicata,N. undata and N. textilis (Prosobranchia: Neritacea) on the rocky shores at Mkomani,Mombasa, Kenya

The vertical zonation of the three common rocky shore neritids at Mkomani, Mombasa, Kenya, Nerita plicata Linnaeus, N. undata Linnaeus, and N. textilis Dillwyn, as a function of feeding migrations and of size, was studied from 28 February to 24 March 1983. These snails perform feeding migrations at night starting at around mid-ebb tide and return to their resting positions with the flood tide. They remain in their resting positions throughout the day until the next nocturnal ebb tide. The direction of migration is sizerelated, with the larger snails of each species moving in the opposite vertical direction to the smaller ones, so that the populations as a whole exhibit no statistically significant net vertical displacement. The larger individuals of two of the species, N. plicata and N. undata, invariably move downwards to their feeding levels, while the smaller individuals move upwards; the larger individuals of N. textilis display a different pattern of migration, moving downwards on and around spring-tide days and upwards on and around neap tide days, while the smaller individuals move in the opposite directions. N. textilis rest above their feeding level around spring tides, and below that level around neap tides. It is demonstrated how these nocturnal migratory feeding rhythms are integrated into the spring-neap and seasonal cycles of the snails' daytime resting positions. The adaptive significance of these migrations is also discussed.