Temperature and salinity: two climate change stressors affecting early development of the New Zealand sea urchin Evechinus chloroticus

Temperature and salinity are important environmental factors affecting the normal functioning of marine animals, particularly animals such as sea urchins living in shallow waters and tide pools. Here, we evaluated the effect of different combinations of temperature and salinity on early embryos of the endemic New Zealand sea urchin Evechinus chloroticus. Animals were collected at Matheson’s Bay (36º18′17′′S; 174º47′51′′E) in north-eastern New Zealand in February 2013. Embryos were exposed to five salinities (29, 31, 34, 35 and 37 ppt) and two temperatures (18 and 21 °C) during the first 24 h of development. Low salinity (29 ppt) affected all parameters (fertilization, development rate, gastrulation and normal development), with ca. 50 % of embryos surviving at 29 ppt, whereas seawater temperature only affected development rate and gastrulation. An increase in temperature from 18 to 21 °C minimized the negative effect of low salinity (≤31 ppt) on development rate and gastrulation of E. chloroticus. Overall, the results of this study suggest that early embryos of E. chloroticus have developmental plasticity to withstand reductions in salinity up to 29 ppt; however, it is still unknown whether the surviving embryos will be able to complete larval development at low salinities, particularly whether the embryos and larvae are carried into extreme environments such as estuaries where salinity is even lower. Multistressor studies are very important for climate change research as multiple environmental factors will act together in the wild, having major consequences for development and recruitment of marine invertebrates.     

Resource allocation and growth rates in the sea urchin Evechinus chloroticus (Echinoidea: Echinometridae)

The morphometry of the sea urchin Evechinus chloroticus from habitats of contrasting algal abundance but of similar urchin density was examined at two localities in southern New Zealand during 1993. Populations from habitats of high algal abundance (Dusky Sound) had similar relationships of demipyramid (jaws) to test diameter, but individuals had significantly smaller jaws relative to their test diameter than those from a locality where algal abundance was low (Arapawa Island). The body wall mass (in relation to total wet weight) was similar for populations from both localities but, for Dusky Sound populations, individuals from exposed sites had greater relative body mass than those from sheltered sites. The ratios of gonad weight:total weight were similar between localities. However, E. chloroticus from Arapawa Island reached reproductive maturity at a smaller size than those from Dusky Sound. Growth rates of E. chloroticus varied among localities in Dusky Sound. Growth was modelled by the Tanaka function, which allows for rapid early growth until reproductive maturity is reached and declining growth rates thereafter. The results show that sea urchins respond to low resource availability by increasing the size of the food-gathering apparatus, maturing at a smaller size, and growing to a smaller size than individuals from food-rich habitats. Received: 3 December 1996 / Accepted: 29 January 1997     

Mass spawning by the sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) in a New Zealand fiord

A mass synchronous spawning of the sea urchin Evechinus chloroticus (Valenciennes) was observed in situ in Doubtful Sound, a large New Zealand fiord. Spawning occurred between 17:30 hrs and 18:30 hrs on 27 January 1994 and coincided with a full moon, spring tides and a period of decreasing sea temperatures. During spawning, the sea urchins formed a dense spawning aggregation of both sexes, with >90% of the urchins observed spawning at the time. Spawned gametes clouded the water column, and some were eaten by small labrid fish species. The spawning, which may have been as widespread as 40 km, marked a 42 to 50% decrease in gonad indices and resulted in a widespread, dense cohort of  E. chloroticus larvae within the fiord. Received: 25 September 1997 / Accepted: 6 March 1998     

Reproductive variability over a four-year period in the sea urchin Evechinus chloroticus (Echinoidea: Echinodermata) from differing habitats in New Zealand

 The endemic New Zealand echinoid, Evechinus chloroticus (Valenciennes), was sampled approximately monthly from September 1990 to October 1994 at three sites in Tory Channel, Marlborough Sounds, New Zealand. These channel sites (outer, mid and inner) were up to 20 km from the open ocean and differed in their shore type, exposure to wave action and macrophyte abundance. E. chloroticus showed an annual reproductive cycle at each site, with gametogenesis commencing in the late austral winter and spawning in summer. Maximum gonad indices (reproductive potential) varied spatially, with the outer site generally having higher maximum gonad indices than the inner site, and temporally, with maximum gonad indices occurring earlier in 3 of the 4 seasons at the outer site than the inner site. The mid and inner sites showed much greater variation in maximum gonad indices (range 15.83 to 26.99% and 11.87 to 20.90%, respectively) than the outer site (range 19.31 to 22.95%). Reproductive output (weight of gametes released per gram echinoid) also varied, with the different sites showing significantly different outputs in the different years. A regression of maximum reproductive potential against reproductive output was significant ( p < 0.001), and had a positive slope with an r ² of 0.79. While, the initiation of gametogenesis was relatively synchronous between sites and years, and is possibly cued by increasing daylength, it progressed at different rates among populations. Spawning did show spatial and temporal variability, occurring near the time of highest sea-surface temperatures (∼15 °C). The observed variations in reproductive cycle may be related to small-scale variability in diet and environmental conditions. Furthermore, asynchronous spawning, variable spawning duration, and variable reproductive output are likely to strongly influence annual recruitment variability in E. chloroticus, with different larval subpopulations contributing unequally in different years. The ecological consequences of this, both for the ability of E. chloroticus to propagate itself in space and time and for the management of the developing E. chloroticus fishery in New Zealand, are discussed. Received: 9 December 1998 / Accepted: 13 June 2000     

Mycosporine-like amino acids prevent UVB-induced abnormalities during early development of the green sea urchin Strongylocentrotus droebachiensis

Experiments were performed to determine how ultraviolet radiation (UVR) in the environmentally relevant range affects development of the sea urchin Strongylocentrotus droebachiensis (Müller) and whether mycosporine-like amino acids (MAAs), present in the early life stages, reduce UV-induced damage. Eggs, embryos, and larvae contained five MAAs having absorption maxima ranging from 320 to 334 nm. Eggs contained principally shinorine and porphyra-334, which absorb maximally at 334 nm and half-maximally at 312 and 348 nm, spanning much of the environmental range of biologically effective UVR. Concentrations of MAAs remained constant in unirradiated embryos through the gastrula stage, but decreased significantly in two-armed pluteus larvae. Daily exposure to combined photosynthetically active radiation (PAR, 400–700 nm) and UVR did not affect the concentration of MAAs in these embryos up to the two-armed pluteus stage. Prism larvae of sea urchins and the sand dollar Echinarachnius parma (Lamarck) did not accumulate shinorine from the surrounding seawater. Daily exposure of embryos to UVA (320–400 nm) and UVB (295–320 nm) radiation in the presence of PAR induced delays and abnormalities during development, and removing UVB eliminated this effect. Abnormalities in embryos included thickening of the blastoderm wall, filling of the blastocoel by abnormal cells, exogastrulation, and formation of abnormal spicules. The percentage of embryos that developed normally was lower in batches of embryos exposed to PAR + UVA + UVB, except in embryos from urchins maintained on MAA-rich diets. In all cases, the percentage of PAR + UVA + UVB-exposed embryos that developed normally was positively related to the concentration of MAAs in eggs from which the embryos developed. Thus, the MAAs found in S. droebachiensis embryos protect them against UVB-induced abnormalities during their development to at least the four-armed pluteus larval stage. Received: 8 May 2000 / Accepted: 29 September 2000     

Limited effects of Antarctic ozone depletion on sea urchin development

The sea urchin, Sterechinus neumayeri, has a circumpolar distribution and is an abundant species in benthic communities of the Antarctic. Reproduction occurs during austral spring, when ozone concentrations over the past 25 years have been reduced by 50% or more, potentially exposing the planktonic embryos and larvae to elevated levels of UVB. During spring of 1996, cultures of S. neumayeri embryos incubated under ambient and partitioned sunlight (minus UVB) at static depths between 0 and 7 m were analyzed for DNA damage [cyclobutane pyrimidine dimers (CPDs)] and morphological abnormalities. At 0-m and 1-m depths, nearly 100% of embryos developed abnormally, even under UVB-shielded conditions where little or no DNA damage accumulated. At depths >3 m, reduced or no abnormality was evident and DNA damage was negligible. Although UVB contributed to 0–65% of solar-induced abnormalities, the mean contribution was 11±17% and UVB was not primarily responsible for observed defects in urchin development. Moreover, developmental responses were not linearly related to ambient UVB gradients as might be expected, but are better characterized relative to threshold levels of total UVB exposure. Accumulated exposures of 25 kJ m^–2 ambient UVB caused minimal DNA damage and allowed normal embryological development to proceed. Higher UVB exposures (especially 80 kJ m^–2) precluded normal development. An ancillary threshold limit of 17 CPDs mb^–1 has been identified as the level of DNA damage that proscribes abnormal development. While higher wavelengths of UVA and visible light are not affected by ozone concentration and do not initiate significant CPD DNA damage, they did interfere significantly with the embryological development of S. neumayeri. It is concluded that exposure to increased UVB during recent Antarctic ozone-depletion cycles probably has only a small degree of impact relative to the magnitude of other solar effects on the developmental success of Sterechinus embryos, or compared to spawning seasons before ozone depletion (i.e., years prior to 1978).Communicated by P.W. Sammarco, Chauvin     

Oxygen and acid-base status of the sea urchin Psammechinus miliaris during environmental hypoxia

The respiratory and acid-base responses to hypoxia of the sea urchin Psammechinus miliaris Gmelin have been studied both in the laboratory and in the field. Sea urchins were collected from the Clyde Sea area, Scotland, between March and July 1993. Individual urchins were unable to regulate their oxygen uptake during hypoxia. The partial pressure of oxygen (P_{O 2}) in the coelomic fluid was lower than ambient P_{O 2} during normoxia but still decreased with a decrease in environmental P_{O 2}. There was a significant increase in pH and in the concentrations of bicarbonate, magnesium and calcium in the coelomic fluid, but a significant decrease in the partial pressure of carbon dioxide (P_{CO 2}), in response to declining P_{O 2}s. The disturbance of respiratory parameters in urchins accompanying hypoxic exposure in rock pools was similar to that observed in the laboratory, although not as severe as might have been expected on the basis of the laboratory experiments.     

Effects of ethynylestradiol and bisphenol A on the development of sea urchin embryos and juveniles

The effects of various concentrations of a synthetic estrogen, ethynylestradiol (EER), and an estrogenic compound, bisphenol A (BPA), on the development of two sea urchin species, Hemicentrotus pulcherrimus and Strongylocentrotus nudus, were examined. At concentrations of 2.5 μM or higher of EER the zygotes did not hatch; at 0.98–1.25 μM they developed but had abnormal morphology; and at concentrations lower than 1 μM there was no effect on embryogenesis. The dose dependency was the same for both species, but more embryos of S. nudus showed exogastrulation at 3–10 μM EER. The effect of BPA on early development was less remarkable than that of EER; most embryos developed normally even in the presence of 2.5 μM BPA. The feeding larvae progressed and finally metamorphosed into juveniles even at 0.1–3 μM EER. The chemicals had opposing effects on the growth of the juveniles. A low dose of EER (0.1–1 μM) promoted growth and the average diameter of the test was bigger than that of the control group; the same dose of BPA suppressed growth and the test was smaller than that of the control group. These results show that the sensitivity and response to endocrine disrupter chemicals changes markedly during the ontogeny of sea urchins. Physical and Chemical Impacts on Marine Organisms, a Bilateral Seminar Italy-Japan held in November 2004     

Development of the echinothurid sea urchin Asthenosoma ijimai

Development of an echinothurid sea urchin is described for the first time; eggs of Asthenosoma ijimai (Yoshiwara) have been fertilized in the laboratory, and development has been followed light-microscopically up to the early juvenile stage. The eggs, which are orange and float, are 1.2 mm in diameter, by far the largest echinoid eggs on record. The embryos, larvae and early juveniles are lecithotrophic, and no exogenous food is needed for development. The embryonic stages include a remarkable biscuit-shaped late blastula, which has never been described for any echinoid before. The larva, with its para-arms unsupported by skeletal ossicles, is unlike the echinoid prism or pluteus and more resembles the early bipinnaria or early auricularia of asteroids and holothurians, respectively. All stages through late larvae float just beneath the surface until settlement occurs during the third and fourth weeks at 20°C. Metamorphosis from late larva to juvenile is gradual and no part of the larval body appears to be cast off.This paper is dedicated to Professor Juro Ishida on the occasion of his seventieth birthday.     

Antigenic specificity of the sea urchin sperm surface

The antigenic composition of the sperm surface in Paracentrotus lividus Lam. and Sphaerechinus granularis Lam. was studied using the sperm agglutination test with homologous and heterologous antisera. The results indicated that sperm of both species have at least one antigenic determinant located on their surface and shared by both species. In addition, Paracentrotus sperm bear at least one species specific determinant on their surface. The existence of antigenic determinants common to gametes of both species was demonstrated.     

Seasonality of feeding and nutritional status during the austral winter in the Antarctic sea urchin Sterechinus neumayeri

The seasonal pattern of food intake and tissue energy status was measured over a 2 year period for two populations of the common Antarctic echinoid Sterechinus neumayeri living on contrasting substrata at Rothera Point, Adelaide Island, Antarctica. Food intake was estimated from faecal egestion, and both tissue mass and energy content assessed. Food availability was intensely seasonal, in that water column chlorophyll content and sediment pigment content varied markedly throughout the year. In response, both urchin populations showed an extremely seasonal cycle of faecal egestion, indicating a strong seasonality of feeding activity. Urchins from North Cove living on soft sediment fed at a considerably higher rate, and had a significantly larger Aristotle's lantern, than those in South Cove, 1 km away, living on hard substrata and taking a more cosmopolitan diet. Faecal egestion in both populations was zero for a 7 month period in the austral winter of 1997, and again for a 4 month period in 1998. During the austral summer of 1997/1998, 84% of the total annual energy intake took place in the period January to March. Significant decrease in gut tissue mass provided energy for maintenance in early winter, although progressive reduction of both gonad energy content (but without a detectable change in gonad mass) and body wall organic mass provided energy during the late winter period. The mass of reproductive tissue showed large differences between the two sites, but there was no marked decrease associated with spawning. Tissue proximate composition was assessed stoichiometrically from elemental composition and also checked by direct assay; gonad tissue was richer in lipid than gut tissue, though both were dominated by protein and contained only small amounts of carbohydrate. These data suggest that the very strong seasonality of food intake does not pose a significant energetic challenge for this species.     

Circulation of perivisceral fluid in the sea urchin Lytechinus variegatus

The principal driving mechanism of perivisceral-fluid circulation was investigated in the echinoid Lytechinus variegatus by metal-clad hot-wire anemometry. Analysis of 23 flow profiles from 13 individuals collected from 1 to 3 m water depth at Tarpon Springs and Sarasota, Florida (USA) in 1984 indicates that for this species, the ciliated epithelium is an ineffective driving mechanism for mixing of the perivisceral fluid. Instead, the Aristotle's lantern is the major driving force of circulation of the perivisceral fluid, with velocity fluctuations of 1.5 mm s^-1 amplitude in the cavity center during intermittent periods of activity. These fluctuations rapidly decay as the ciliated surfaces are approached. Spectral analysis of velocity time-series reveals predominant energy-containing velocity fluctuations between 0.007 and 0.05 Hz. The circulation, which can be described as non-turbulent forced mixing, has revealed four different flow patterns which appear to be correlated with specific animal activities. A modified eddydiffusion model predicts that oxygen transport through the cavity over a 2 cm path length requires more than 20 h. Calculation of the oxygen flux to a ripe ovary suggests that supply does not meet ovarian oxygen demand in this case. Alternative pathways of oxygen transport invoking advection in perivisceral-fluid eddies and along the ciliated coelomic surfaces are compatible with the observed flow patterns and lead to much shorter oxygen-transport time scales of the order of 1 to 10 min.     

Experimental evaluation of aggregation behavior in the sea urchin Strongylocentrotus droebachiensis

Defensive aggregation by Strongylocentrotus droebachiensis has been invoked as the fulcrum for the transformation of macroalgal beds into coralline barrens in the northwest Atlantic. We critically examined some of the mechanisms contributing to aggregation behavior by experimentally manipulating sea urchins, purported predators and food during autumn 1983 and spring 1984 both in the laboratory and field. We utilized several approaches to examine a range of sea urchin responses to the presence of food, tethered predators, caged predators, crushed con-specifics in the field and predators in laboratory tanks. Some of the field cages had the property of allowing free passage to sea urchins while retaining lobsters; this allowed distinctions to be made between artifacts caused by cage walls or topographic barriers and unrestricted behavioral responses of sea urchins. The results falsified the hypothesis that aggregations of S. droebachiensis are elicited by predators. Except in the presence of algae, sea urchins always avoided decapod predators (but not sea stars) and fled from the vicinity of injured conspecifics. However, avoidance behavior was subordinate to feeding responses, demonstrated by mass migrations of sea urchins into cages (with lobsters) to feed on algae. We reaffirmed by observation and manipulation previous studies which showed that sea urchins aggregate only in the presence of food. Two types of sea urchin groupings were delineated: (1) surficial two dimensional associations, often caused by topographic or other features which inhibited dispersal and (2) cohesive three-dimensional aggregations induced by food.     

Removal of glycine from solution by the sea urchin Strongylocentrotus purpuratus

Radioautography and liquid-scintillation counting of juvenile sea urchins — Strongylocentrotus purpuratus (Stimpson) — exposed to ³H- and ¹⁴C-labeled glycine showed that the ³H is rapidly translocated throughout the animal and lost, while the ¹⁴C is slowly translocated into the interior of the urchin and incorporated into insoluble material.     

Effects of sea urchin disease on coastal marine ecosystems

Outbreaks of disease in herbivorous sea urchins have led to ecosystem phase shifts from urchin barrens to kelp beds (forests) on temperate rocky reefs, and from coral to macroalgal-dominated reefs in the tropics. We analyzed temporal patterns in epizootics that cause mass mortality of sea urchins, and consequent phase shifts, based on published records over a 42-year period (1970–2012). We found no evidence for a general increase in disease outbreaks among seven species of ecologically important and intensively studied sea urchins. Periodic waves of recurrent amoebic disease of Strongylocentrotus droebachiensis in Nova Scotia coincide with periods when the system was in a barrens state and appear to have increased in frequency. In contrast, following a major epizootic that decimated Diadema antillarum throughout the Caribbean in 1983, subsequent outbreaks of disease were highly localized and none have been reported since 1991. Epizootics of Strongylocentrotus in the NW Atlantic and NE Pacific, and Paracentrotus and Diadema in the eastern Atlantic, have been linked to climate change and overfishing of sea urchin predators. The spatial extent of recurrent disease outbreaks in these species, and the frequency of phase shifts associated with these epizootics, has decreased over time due to the expansion of the macroalgal state and its stabilization through positive feedback mechanisms. Longitudinal studies to monitor disease outbreaks in sea urchin populations and improved techniques to identify causative agents are needed to assess changes in the frequency and extent of epizootics, which can profoundly affect the structure and functioning of coastal marine ecosystems.     

Changes in sea urchin populations after the destruction of kelp beds

In St. Margaret's Bay, Nova Scotia, Canada, there are large areas in which sea urchins (Strongylocentrotus droebachiensis) have eliminated beds of kelp (Laminaria spp.). Sites were identified where destruction of kelp beds had taken place 1, 2, 3, 3.5 and 4 years ago. With increase of time since kelp disappearance, the sea urchins showed decreased growth rate, reduced gonad size, but an increase in numbers resulting from high recruitment rates in the first two years after kelp bed destruction. These sea urchin populations, by their browsing, effectively prevent the regeneration of kelp. There is, as yet, no evidence of the sea urchin populations being starved out to allow the kelp to return.