Random movement pattern of the sea urchin Strongylocentrotus droebachiensis

We describe the fine-scale movement of the sea urchin Strongylocentrotus droebachiensis based on analyses of video recordings of undisturbed individuals in the two habitats which mainly differed in food availability, urchin barrens and grazing front. Urchin activity decreased as urchin density increased. Individuals alternated between moving and being stationary and their behaviour did not appear to be affected by either current velocity (within the range from 0 to 15 cm s^− 1) and temperature (2.3 to 6.0 °C). Movement of individuals at each location was compared to that predicted by a random walk model. Mean move length (linear distance between two stationary periods), turning angle and net squared displacement were calculated for each individual. The distribution of turning angles was uniform at each location and there was no evidence of a relationship between urchin density and either move length or urchin velocity. The random model predicted a higher dispersal rate at locations with low urchin densities, such as barrens habitats. However, the movement was sometimes greater or less than predicted by the model, suggesting the influence of local environmental factors. The deviation of individual paths from the model revealed that urchins can be stationary or adopt a local (displacement less than random), random or directional movement. The net daily distance displaced on the barrens, predicted by a random walk model, was similar to the observed movement recorded in our previous study of tagged urchins at one site, but less than that observed at a second site. We postulate that the random dispersal of urchins allows individuals on barrens to reach the kelp zone where food is more abundant although the time required to reach the kelp zone may be considerable (months to years). Urchins decrease their rate of dispersal once they reach the kelp zone so that they likely remain close to this abundant food sources for long periods.     

Settlement behaviour and early post-settlement predation of the sea urchin Strongylocentrotus droebachiensis

We examined behaviour of competent larvae of the green sea urchin Strongylocentrotus droebachiensis provided with pebbles encrusted with coralline red algae, a strong settlement inducer, in laboratory experiments. Larvae settled at greater frequencies on upward-facing coralline surfaces and in small gaps between coralline and glass surfaces than expected by a random distribution of settlement. These patterns may be explained by encounter rate with inductive cues. There was no change in settler distributions within ~ 1 week of settlement, indicating no net movement between adjacent microhabitats. In flow, live and recently killed larvae settled or were passively entrapped at greater frequencies on high- than low-rugosity coralline crusts. Recent settlers (0.5-1 mm test diameter) were consumed by small decapod crustaceans and bulldozed by periwinkles. Juveniles became less vulnerable to predation by hermit crabs with increasing size, and reached a growth refuge at ~ 10 mm test diameter. Our laboratory findings suggest that the cryptic distribution of recent settlers is probably not due to microhabitat selection by settling larvae or early post-settlement migration, at least not in response to physical cues such as light or surface texture. Differential rates predation of young juveniles between exposed and cryptic habitats cannot be ruled out as an important determinant of this pattern.     

The effect of the quality of food patches on larval vertical distribution of the sea urchins Lytechinus variegatus (Lamarck) and Strongylocentrotus droebachiensis (Mueller)

Although most invertebrate larvae are weak swimmers and act as passive particles on horizontal scales, they may be able to regulate their vertical position in response to different factors, including increased food concentration. We examined the effect of the quality of food patches on larval vertical distribution for the sea urchins Lytechinus variegatus and Strongylocentrotus droebachiensis, and determined the effect of dietary conditioning on that response in the laboratory. We reared larvae on a mixed algal diet of Dunaliella tertiolecta and Isochrysis galbana under low (500 cells ml⁻¹) and high (5000 cells ml⁻¹) rations. Food patches were maintained in Plexiglas rectangular columns (30×10×10 cm) using a density gradient, where practical salinity in the bottom layer was 33, in the middle layer 30, and in the top layer 27. We examined the magnitude and mechanism of a behavioural response of larvae of L. variegatus in the four-arm stage, and on two developmental stages of S. droebachiensis (four- and six-arm), by manipulating patch quality. In the absence of a patch, larvae of both species and developmental stages swam through to the surface of the experimental columns. In the presence of algae, fewer larvae were present above the patch and more were at the patch than in control columns. More larvae swam through patches of “unflavoured” algal mimics than algal patches, and aggregated at the surface. Larval distribution relative to patches of algal filtrate without algal cells or of “flavoured” algal mimics in algal filtrate was not consistently different from that in either control or algal patches; thus, the magnitude of larval response to filtrate (with or without particles) was intermediate between that to control and algal patches. For L. variegatus, more larvae crossed the patches when reared on low than high rations, indicating that poorly conditioned larvae may be less responsive to environmental cues. Our results suggest that larvae can actively aggregate and maintain a vertical position in response to a food patch that depends on the quality and quantity of food. The response appears to be based mostly on a chemosensory rather than a mechanosensory mechanism.     

Effect of dietary history and algal traits on feeding rate and food preference in the green sea urchin Strongylocentrotus droebachiensis

Feeding behaviour is influenced by a variety of factors, including nutritional requirements, the quality of available foods, and environmental conditions. We examined the effect of two factors, food morphology and dietary history, on the feeding rate and preference of the sea urchin Strongylocentrotus droebachiensis. Standardizing food shape and structure did not alter urchins' expected preference for the native kelp Laminaria longicruris over the invasive alga Codium fragile ssp. tomentosoides. However, when foods containing L. longicuris were shaped to mimic the algae, the C. fragile mimic was consumed more rapidly than the kelp mimic. Dietary history had no effect on single diet feeding rate. Urchins feeding on C. fragile consistently consumed twice as much (by mass) as those fed kelp, regardless of their previous diet. Despite higher feeding rates on C. fragile, urchins feeding on this alga were unable to compensate for its low energetic content and ingested less energy. Dietary history had a short-term effect on food preference, with urchins tending to prefer less familiar foods. Our findings suggest that urchins feed on C. fragile at a high rate, due to ease of handling and/or compensatory feeding, and that they do not a have strict preference hierarchy. Rather, food choice appears to reflect active maintenance of a mixed diet.     

Developmental plasticity in larval development in the echinometrid sea urchin Evechinus chloroticus with varying food ration

Developmental plasticity in the morphology of planktotrophic echinoid larvae has been studied primarily in temperate sea urchins from the Northern Hemisphere. These studies have shown that echinoplutei with reduced food ration generally respond by increasing the length of the larval arms, and thus the length of the ciliated band, and delaying formation of the rudiment. Using the endemic New Zealand sea urchin Evechinus chloroticus we tested for the presence of developmental plasticity in larvae fed a high or low algal food ration (6000 or 600 Dunaliella cells/ml), or with no algal food. Our results show that developmental plasticity in larval form is seen in a Southern Hemisphere representative of the Family Echinometridae, but the general pattern of longer arms with low food ration was only seen in the earliest part of development. Larvae in the High food treatment were largest in all dimensions and formed rudiments within 23 days of fertilization. Larvae fed a low algal ration or no algal food stalled at the four-arm echinopluteus stage, and were significantly smaller in size, and differed in shape, when compared in a multivariate analysis to the High food treatment. We suggest that the response of echinoplutei to low levels of particulate food is a species-specific trait, depending in part on the level of dependence of the larvae on exogenous food. Previous studies in Lytechinus variegatus, and the present study with E. chloroticus, suggest that in species where development stalls at the four-arm stage, the pattern of longer larval arms with low food ration will only be seen during the initial early period of larval growth. Additionally our results show that there can be significant variation in larval morphology between replicate jars in the same feeding treatment, suggesting that future research on developmental plasticity should also consider differences in larval morphology between culture containers.     

The effects of thin layers on the vertical distribution of larval Pacific herring, Clupea pallasi

Temporal and spatial heterogeneity of resources is likely to have dramatic effects on the behaviors of zooplankton and ichthyoplankton, which in turn are likely to have strong effects on ecological dynamics such as predation, growth, and mating. The objective of this study was to determine whether vertically thin layers of extreme prey concentration affect the vertical distribution of larval Pacific herring (Clupea pallasi). We employed 2-m tall experimental tanks equipped with video cameras that scanned the vertical extent of the tanks to investigate the effects of thin layers on the vertical distribution of 5- and 10-day-old herring larvae. Three treatments were established: (1) a thin layer of prey (rotifers, Brachionus plicatilis) through density (salinity) stratification, (2) homogeneous vertical distribution of both prey and density, and (3) density (salinity) stratification, but with a homogeneous distribution of prey. We found that in all treatments the majority of larval herring were at the surface, near the light, despite the absence of a peak in rotifer abundance at this depth in some instances. However, there were also clear effects of the thin layers—secondary subsurface peaks in herring abundance occurred at the mid-depths in the stratified tanks, in and around the thin layers. In addition, our results provide some evidence that thin layers specifically, rather than prey patches generally, influence the vertical distribution of larval herring, i.e., larvae may use the physical properties of thin layers to locate and distribute themselves, instead of reacting solely to the prey patches. Thus thin layers can affect directly the vertical distribution of larval herring, and perhaps indirectly their horizontal distribution, as herring larvae live in environments (e.g., estuaries) where advective transport is also often vertically heterogeneous.     

The effects of thin layers on the vertical distribution of the rotifer, Brachionus plicatilis

Microscale patches of resources occur in both the horizontal and vertical dimensions, and in the latter case are referred to as thin layers. These layers may affect ecological processes like behavior, predation, growth and reproduction in phytoplankton and zooplankton. The objective of this study was to determine possible effects of physical and biological thin layers on the vertical distribution and diel vertical migration of the rotifer Brachionus plicatilis. We used four, 2 m tall, experimental tanks fitted with video cameras which panned the vertical extent of each tank and enabled us to sample on the centimeter scale. The experimental tanks consisted of a thin layer (25 cm thick) of Nannochloropsis oculata, whereas control tanks consisted of homogeneously distributed algae. Rotifers aggregated in the thin layers of N. oculata, and dispersed (becoming evenly distributed) after depleting the algae within the thin layer (ca. 6 h). In contrast, rotifer aggregation in the physical thin layer of control tanks was shorter in duration (ca. 2.5 h) and rotifers were homogenously distributed for the remainder of the experiment despite persistent salinity stratification. No signs of diel vertical migration were noted in either experimental or control tanks. A second set of experiments was run to examine the response of rotifers to a choice of food, i.e., thin layers of the diatom, Skeletonema costatum versus the eustigmatophyte, N. oculata. For the choice experiments, two thin layers were created, one with each food option. Our results suggest that B. plicatilis aggregates and feeds preferentially on N. oculata over S. costatum. In both types of experiments rotifers responded, in terms of distribution, to thin layers of algae within the first half-hour of introduction and remained in the thin layers until the food source was depleted. Our results suggest that rotifers may be important grazers on thin layers because of their ability to quickly locate and take advantage of ephemeral food patches.     

Relative importance of parental and larval nutrition on larval development and metamorphosis of the sea urchin Strongylocentrotus droebachiensis

We examined the relative importance of parental nutritional condition and larval food ration on the rates of development, growth and metamorphosis of larvae of Strongylocentrotus droebachiensis (Müller) in a laboratory experiment. Parents were reared for 22 months on either a high ration of kelp (Laminaria spp., 6 days week⁻¹) supplemented with mussel flesh (Mytilus spp., 1 day week⁻¹) (KM), or a low ration of kelp (1 day week⁻¹) (KL). Larvae were fed either a high ration (5000 cells ml⁻¹) or a low ration (500 cells ml⁻¹) of microalgae (Dunaliella tertiolecta). Larval food ration had a strong effect on the rates of development, growth, and metamorphosis, which were all significantly greater in larvae fed the high ration. Test diameter of settlers also was significantly greater in the high than the low ration. Parental nutritional condition had little or no effect on the rates of development and growth, and no effect on settler size. The rate of metamorphosis was significantly higher in larvae from the KM than the KL treatment in the high but not the low ration (where rates of metamorphosis were similar). Although parental condition generally had a small effect on larval development, our results suggest that when planktonic food is abundant, larvae of adults from nutritionally rich habitats (such as kelp beds) may metamorphose sooner than those of adults from nutritionally poor habitats (such as barrens).     

Social behaviour of juvenile red sea urchins, Strongylocentrotus franciscanus (Agassiz)

This study examined social behaviour of juvenile red sea urchins, Strongylocentrotus franciscanus (Agassiz). At four coastal locations in British Columbia, Canada, distributions of juvenile sea urchins were examined in relation to adults. One-third of all juveniles were found underneath an adult “spine canopy”, another third outside the spine canopy but close to an adult, and the remainder were found apart from adults. Juveniles associated with adults were contagiously distributed with each other. In the laboratory, juveniles chose adults over other target locations. They selected adults in particular locations over others, and in one case showed selection among adults; but they did not select between fed and non-fed adults, nor between adults that had been “protective” and “non-protective” of juveniles in the field. In time-lapse film studies, starved juveniles showed little change in social behaviour when food was introduced, but showed a dramatic change in behaviour when predators were active. We suggest that juvenile red sea urchins are found under the spine canopies of adults as a result of juvenile behaviour; and that this interaction functions to protect juveniles from predation. The strong gregarious nature of juveniles among themselves may have evolved in a different selective situation as a defence against predation and to ensure reproductive success.     

Developmental cis-regulatory analysis of the cyclin D gene in the sea urchin Strongylocentrotus purpuratus

Cyclin D genes regulate the cell cycle, growth and differentiation in response to intercellular signaling. While the promoters of vertebrate cyclin D genes have been analyzed, the cis-regulatory sequences across an entire cyclin D locus have not. Doing so would increase understanding of how cyclin D genes respond to the regulatory states established by developmental gene regulatory networks, linking cell cycle and growth control to the ontogenetic program. Therefore, we conducted a cis-regulatory analysis on the cyclin D gene, SpcycD, of the sea urchin, Strongylocentrotus purpuratus, during embryogenesis, identifying upstream and intronic sequences, located within six defined regions bearing one or more cis-regulatory modules each.     

Exposure to ultraviolet radiation causes proteomic changes in embryos of the purple sea urchin, Strongylocentrotus purpuratus

We performed experiments to determine how environmentally relevant ultraviolet radiation (UVR) affects protein expression during early development in the sea urchin, Strongylocentrotus purpuratus. To model the protein-mediated cell cycle response to UV-irradiation, six batches of embryos were exposed to UVR, monitored for both delays in the first mitotic division and changes in the proteome at two specific developmental time points. Embryos were exposed to or protected from artificial UVR (11.5 W/m²) for 25 or 60 min. These levels of UVR are within the range we have measured in coastal waters between 0.5 and 2 m. Embryos treated with UVR for 60 min cleaved an average of 23.2 min (± 1.92 s.e.m.) after UV-protected embryos. Differential protein spot migration between UV-protected and UV-treated embryos was examined at 30 and 90 min post-fertilization using two-dimensional SDS-PAGE (2D GE). A total of 1306 protein spots were detected in all gels, including differences in 171 protein spots (13% of the detected proteome) in UV-treated embryos at 30 min post-fertilization and 187 spots (14%) at 90 min post-fertilization (2-way ANOVA, P = 0.03, n = 6). The majority of the proteins affected by UVR were subsequently identified using matrix assisted laser desorption ionization tandem time-of-flight mass spectrometry (MALDI-TOF-TOF MS). Our results indicate UVR affects proteins from multiple cellular pathways and indicate that the mechanisms involved in UV-stress and UV-induced developmental delay in sea urchin embryos are integrated among multiple pathways for cellular stress, protein turnover and translation, signal transduction, cytoskeletal dynamics, and general metabolism.     

The larval stages of the sea urchin, Strongylocentrotus purpuratus

The adult body plan of Strongylocentrotus purpuratus is established within the imaginal rudiment during the larval stages. To facilitate the study of these stages, we have defined a larval staging scheme, which consists of seven stages: Stage I, four-arm stage; Stage II, eight-arm stage; Stage III, vestibular invagination stage; Stage IV, rudiment initiation stage; Stage V, pentagonal disc stage; Stage VI, advanced rudiment stage; and Stage VI, tube-foot protrusion stage. Each stage is characterized by significant morphological features observed for the first time at that stage. This scheme is intended as a guide for determining the degree of larval development, and for identifying larval and adult structures. Larval anatomy was visualized using light and confocal microscopy as required on living material, whole mount fixed specimens, and serial sections. Antibody staining to localize specific gene products was also used. Detailed analysis of these data has furthered our understanding of the morphogenesis of the rudiment, and has suggested provocative questions regarding the molecular basis for these events. We intend this work to be of use to investigators studying gene expression and morphogenesis in postembryonic larvae.     

Impact of CO2-acidified seawater on the extracellular acid-base balance of the northern sea urchin Strongylocentrotus dröebachiensis

We investigated the effect of five day exposure to CO₂-acidified sea water treatments (pH_NBS = 7.89 [control], 7.44, 7.16 and 6.78, T = 9.5 °C) on the extracellular acid-base balance of the northern sea urchin Strongylocentrotus dröebachiensis. In each case there was an uncompensated respiratory acidosis which increased in intensity with decreasing environmental pH. This was very similar to results for another sea urchin species, Psammechinus miliaris (8 d exposure, T = 15 °C). However, there were some important differences in the response to low seawater pH between the two urchin species S. dröebachiensis and P. miliaris. At the lowest pH tested (6.78) there was a metabolic component to this acidosis recorded (correlated with a significant increase in l-lactate) in S. dröebachiensis but not P. miliaris. The acidosis was accompanied by a very small, but significant increase in coelomic fluid calcium. Also the water used in our study was (controlling for pH) markedly undersaturated with respect to carbonate compared with that used in the Psammechinus study, highlighting the need for the environmental context to be assessed in future comparative studies.     

Feeding preference of Strongylocentrotus droebachiensis (Echinoidea) for a dominant native ascidian, Aplidium glabrum, relative to the invasive ascidian Botrylloides violaceus

Subtidal benthic communities show distinct patterns of community structure related to substrate angle. Suspension-feeding invertebrate communities often dominate vertical and undercut rock surfaces, while macroalgae dominate horizontal surfaces. One factor that may shape this pattern is sea urchin grazing, which is often more intense on horizontal surfaces. The native Gulf of Maine ascidian Aplidium glabrum, like other native ascidians, is generally restricted to vertical and undercut rock walls, whereas the introduced ascidian Botrylloides violaceous is often abundant on horizontal surfaces. We tested the hypothesis that this pattern could be due to differing predation intensity on these two ascidians by Strongylocentrotus droebachiensis, a dominant omnivore in the Gulf of Maine. Feeding preference of S. droebachiensis on the native A. glabrum vs. B. violaceous was estimated in the laboratory and in field experiments. Laboratory results show that S. droebachiensis prefers to feed on the native ascidian A. glabrum over B. violaceous. In the field, potential differences in the impact of S. droebachiensis on the two species were masked by the much greater growth rate of B. violaceus compared to A. glabrum. These results may help explain observed patterns in ascidian distribution in the Gulf of Maine, and ultimately the overall success of B. violaceus as a major invader throughout New England.     

The effect of salinity on larval survival and development in the sea urchin Echinometra lucunter

Summary

Reductions in salinity can have adverse effects on larval development and larval survival in some invertebrate taxa but not others. Salinity tolerance of larvae may be particularly important in echinoderms because they are both poor ion regulators and stenohaline. I examined the effect of six levels of salinity (15, 18, 21, 24, 27 and 33 PSU) on survival and rate of development of larvae in the subtropical sea urchin Echinometra lucunter. In the short-term, mortality rate was significantly lower in 33 PSU than in all other salinities except 27 PSU, and it was significantly greater in 15 and 18 PSU than in all higher salinities. In the long-term, daily and cumulative mortality were significantly greater in 15 PSU than in most other salinities over 11 days of development (except for cumulative mortality in 18 PSU). They were significantly greater in 18 PSU than in 21 PSU or 33 PSU over a period of 13 days. Furthermore, daily mortality was significantly greater in 18 PSU than in 24 PSU or 27 PSU at 13 d after fertilization. Daily and cumulative mortality were significantly lower in 33 PSU than in 21, 24 or 27 PSU over a period of 17 days. Although in the control (33 PSU) 75% of larvae completed development to the 8-arm stage at 35 d, no larvae developed further than the 4-arm stage in 18, 21, 24 or 27 PSU; in 15 PSU, ~60% of larvae did not develop further than swimming blastulae. Since prolonged exposure to salinities as high as 27 PSU (frequently recorded in the adult habitat) can result in great larval losses, adaptive behaviours that prevent larvae from entering water layers of low salinity will enhance their chance for survival.     

Changes in growth and reproduction of green sea urchins, Strongylocentrotus droebachiensis (Müller), during repopulation of the shallow subtidal zone after mass mortality

Following a disease outbreak that caused mass mortality of green sea urchins, Strongylocentrotus droebachiensis, along the Atlantic coast of Nova Scotia in September 1999, changes in growth and reproduction were monitored over 3.75 years as surviving individuals migrated from deep water to repopulate the shallow subtidal zone at a wave-exposed site. Urchins were sampled at 4 depth strata: at 24 m on a boulder field where the population was unaffected by the disease, at 12 and 16 m on a steeply sloping bedrock ramp, and at 8-10 m along the lower margin of a kelp bed (Laminaria digitata) where urchins formed a grazing front by January 2002. Urchins migrating shoreward from the deep-water refuge responded rapidly to increased algal productivity in the shallows through increased growth and reproduction. Measures of annual increments of skeletal elements (rotules) from urchins across the depth gradient indicated that the fastest growing individuals from the source population formed the grazing front. Urchins in the front reached a larger asymptotic size and produced larger gonads than urchins lower on the ramp. The annual cycle in gonad index showed a pronounced spring spawning period across all depths; a secondary fall spawning was evident at the front and 12 m. The presence of mature, fertilizable ova and short response time to spawning induction in both spring and fall supported the occurrence of two spawning periods.     

Horizontal and vertical distribution of meiofauna on sandy beaches of the North Sea (The Netherlands, Belgium, France)

Sandy intertidal zones were analysed for the presence of meiofauna. The material was collected on six macro-tidal sandy beaches along the North Sea (The Netherlands, France, Belgium), in order to analyse the vertical and horizontal meiofaunal distribution patterns. Eleven higher meiofauna taxa (one represented by larval stage—Copepoda nauplii) were recorded. The maximum total meiofauna abundance was observed on the Dutch beach (4,295±911 ind. 10 cm⁻²) in the Westerschelde estuary, while the lowest values (361±128 ind. 10 cm⁻²) were recorded in France at the Audresselles beach. Meiofauna of the different localities consisted mainly of nematodes, harpacticoids and turbellarians. Nematodes numerically dominated all sampled stations, comprising more than 45% of the total meiofauna density. Meiofauna was mainly concentrated at the sand surface with about 70% present in the uppermost 5 cm. Meiofauna occurred across the entire intertidal zone. A clear zonation pattern in the distribution of meiofauna taxa across the beaches was observed. The present work suggests that designation of exposed sandy beaches as physically controlled (McLachlan 1988) does not explain their biological variability.     

Gonad growth in the sea urchin, Strongylocentrotus purpuratus (Stimpson) (echinodermata: Echinoidea) and the assumptions of gonad index methods

In central Oregon intertidal populations, the echinoid Strongylocentrotus purpuratus (Stimpson) first begins to produce mature gametes at a diameter of 25 mm during the second year of its life. All individuals above 40 mm in diameter have mature gametes during the mid-winter spawning season. Gonad size increases rapidly relative to body size until the animals are ≈45 mm in diameter and have a total dry weight of ≈ 15 g. The ratio of gonad to body size reaches its maximum in animals between 40 mm and 50 mm in diameter; thereafter the ratio drops slightly with increasing size. The curvilinear relation between gonad size and body size is not related to a relative difference in body proportions with size. Internal volume, height, and diameter increase linearly with size. Body proportions did not differ between the two populations studied. Differences between populations in the ratio of gonad to body size extend to all sizes in the populations and the direction but not the amount of the difference is consistent from year to year. These differences between habitats are probably related to food supply. The use of gonad ratio methods to normalize gonad size assumes that, within a given population, animals of different body size have the same ratio of gonad size to body size. This assumption is not correct for four species of sea urchins. Gonad index or ratio methods are useful for comparing animals of the same size through time within a population or from different habitats. Restriction of the size range of animals used and use of samples of sufficient size permit gonad ratios to be used to assess the capacity of different habitats to support gonad production in sea urchins and other animals.