Avoiding predation: alarm responses of Caribbean sea urchins to simulated predation on conspecific and heterospecific sea urchins

Alarm responses to the extracts of conspecifics and hetero-specifics were measured for the Caribbean sea urchins Echinometra viridis, E. lucunter, Lytechinus variegatus, L. williamsi, Tripneustes ventricosus, Diadema antillarum, and Eucidaris tribuloides collected along the Caribbean coast (9°3314N; 78°5523W) during October 1984 and July–December 1985. Responses to seawater and extracts of the gnathostomate echinoid Clypeaster sybdepressus were used as controls. The intensity of the response resulting from exposure to sea-urchin extracts was measured by: (1) the percentage of individuals that responded by moving away from the extract and/or towards shelter, and (2) the mean distance moved. Echinometra viridis, E. lucunter, and L. williamsi responded to sea-urchin extracts by moving towards nearby shelter sites. The distance that individuals of each species moved in the first minute following exposure to conspecific extracts was correlated with the distance that species moved from shelter while foraging. L. variegatus and D. antillarum, living in microhabitats not providing protection from predators, responded to extracts of conspecifics and heterospecifics by moving away from the direction of the extract. Eucidaris tribuloides did not exhibit alarm responses to the extracts of con- or hetero-specifics. E. tribuloides secures itself with its stout spines into protected sites within corals. Similarly, L. variegatus living in long, dense seagrass that provided protection from detection by predators, and D. antillarum occupying crevices, showed no alarm responses to extracts of conspecifics. Presumably, in these situations, sea urchins cannot increase their defenses against predation by moving away from an injured neighbor. T. ventricosus showed a weak response to extracts of L. variegatus, but no response to extracts of other species including conspecifics. The reasons for this lack of an alarm response are unclear. For the five species that demonstrated an alarm response to sea-urchin extracts, the intensity of the response varied depending on the type of extract used. L. variegatus, L. williamsi, and D. antillarum responded most strongly to extracts from conspecifics, while Echinometra viridis and E. lucunter responded strongly to extracts from both conspecifics and congeners. The weakest responses were shown to the extracts of T. ventricosus and Eucidaris tribuloides. Habitat overlap, overlap in predators, and phylogenetic relationships did not consistently explain patterns of alarm responses to the extracts of heterospecific sea urchins.     

Predators of juvenile sea urchins and the effect of habitat refuges

We evaluated the effects of potential predators from intertidal habitats on Strongylocentrotus purpuratus survival using laboratory experiments and assessed abundances of main predatory species along the Pacific coast of North America. The interactive effects of urchins’ and predators’ sizes in mediating predation were quantified. Habitat complexity (substrate pits, adult spine canopy) was manipulated to examine its effects on predation of most susceptible individuals (<14 mm). Pachygrapsus crassipes was identified as a major predator of urchins up to ≈30 mm. A positive effect of predator size on consumption of progressively larger urchins was detected, probably due to a mechanical limitation on crabs’ ability to consume large prey. Larger claws of males with respect to females of comparable sizes facilitated the handling of larger prey. Substrate refuges significantly reduced mortality on juvenile urchins. These results show that crab predation may be important in organizing intertidal communities, despite multiple ecological mechanisms promoting sea urchin survival.     

Short-term temporal patterns of early recruitment of coral reef fishes in the tropical eastern Pacific

Short-term temporal patterns of recruitment have been described in a variety of coral reef fishes and have often been related with lunar and tidal cycles. While the relative importance of lunar and tidal factors in determining recruitment patterns has been difficult to assess, most studies have been done in the Caribbean and Indo-Pacific, where tidal amplitudes are small. We studied the short-term temporal dynamics of fish recruitment at Gorgona Island (tropical eastern Pacific), where there is a large tidal amplitude (~4.4 m). Every other day during three consecutive months in 1998, we directly measured the magnitude of reef fish recruitment to standardized coral units (SCUs) isolated from natural reefs. A total of 40 species from 21 families settled on the SCUs. Of 11 species with sufficient numbers for meaningful statistical analyses, two (Lutjanus guttatus and Pomacanthus zonipectus) had lunar recruitment with peaks near the new moon; three combined species of antennariids showed semilunar recruitment with peaks near moon quarters; and eight other species showed sporadic and aperiodic recruitment pulses. The contribution of lunar (moonlight intensity) and tidal factors (tidal amplitude and net tidal flow) to recruitment dynamics varied among species, although it was generally low (<18%) even among species with periodic patterns, except perhaps in L. guttatus. In this species, recruitment magnitude correlated negatively with moonlight intensity, accounting for 34.5% of the variance. Post-settlement predation by roving predators may be one cause of this relationship. In the remaining species, particularly those with sporadic and aperiodic recruitment pulses, stochastically varying weather and oceanographic events may be more important in determining temporal variation in recruitment.     

Changing lobster abundance and the destruction of kelp beds by sea urchins

In a study area in Nova Scotia, Canada, abundance of the lobster Homarus americanus decreased by nearly 50% in 14 years. The lobster is a major predator of sea urchins, and during the past 6 years the sea urchin Strongylocentrotus droebachiensis has destroyed 70% of the beds of Laminaria spp. in the area. Implications for management are discussed.     

Energetics of early development for the sea urchinsStrongylocentrotus purpuratus andLytechinus pictus and the crustaceanArtemia sp.

Embryos and larvae of two species of sea urchin,Strongylocentrotus purpuratus andLytechinus pictus, and larvae of the brine shrimpArtemia sp. (San Francisco brand) were cultured to investigate the contribution of dissolved organic material in seawater to the energetics of early development. When embroys ofS. purpuratus were reared in artificial seawater, a net loss in dry organic mass was observed. In contrast, when sibling embryos were reared to Day 2 under identical conditions in natural seawater, there was either a net increase in dry organic mass or no change. A net decrease in mass was observed in only one of five cultures reared in filtered natural seawater. Energy budgets for each species were determined by giving energy equivalents to the changes in carbohydrate, lipid and protein, and to the rate of oxygen consumption for each day of development. In the case ofS. purpuratus, the use of endogenous reserves accounted for either 0 or 38% of the metabolic demand for two independent cultures reared from Days 0 to 2. For larvae ofL. pictus, reared to 8 d, only 66% of the metabolic demand could be accounted for by the use of endogenous reserves. Sea urchins are capable of transporting dissolved organic material from seawater. Calculations revealed that the energy deficit during the early development of sea urchins (S. purpuratus) could be accounted for by the uptake of dissolved organic matter from seawater. However, for a species that cannot use this resource (Artemia sp.), the metabolic needs during development are supplied through the use of endogenous reserves.     

The rise of thermophilic sea urchins and the expansion of barren grounds in the Mediterranean Sea

Recent ecological studies have shown a strong relation between temperature, echinoids and their grazing effects on macro-algal communities. In this study, we speculate that climate warming may result in an increasingly favourable environment for the reproduction and development of the sea urchin Arbacia lixula. The relationship between increased A. lixula density and the extent of barren grounds in the Mediterranean Sea is also discussed.     

Phytoplankton production: seasonal change in the oceanic eastern tropical Pacific

The suggestion that the annual cycle of plant production in tropical oceanic regions may be negligible or non-existent is examined, using data from a year-long cruise series in the eastern tropical Pacific. Results of analysis of variance show a highly significant seasonal effect. Average values of the seasonal cycle were found to range from 127 to 318 mg C/m²/day, a systematic two-fold variation over the year. Annual production was 75 g C/m²/year. Significant differences also were found between longitudes, and a slightly significant interaction occurred between season and longitude. Probable sources of the seasonal cycle include time variation of thermocline topography and variation of nutrient supply from local source areas such as the Costa Rica Dome, Gulf of Tehuantepec, Peru Current extension, and Equatorial Undercurrent domain.     

Acid-base status in the sea urchins Psammechinus miliaris and Echinus esculentus (Echinodermata: Echinoidea) during emersion

The acid-base status of two sea urchins, Psammechinus miliaris (Gmelin) and Echinus esculentus (L.) during experimental emersion has been investigated. Sea urchins were collected from the Firth of Clyde between August and September 1987. The carbon dioxide capacity of the coelomic fluid of P. miliaris was greater than that of E. esculentus, although both were low and only marginally greater than that of sea water. The pH of the coelonic fluid was also low (7.05 to 7.17) and was influenced mainly by the internal partial pressure of CO₂ (P_{CO 2}). Acid-base disturbance in the coelomic fluid of both species during emersion, although minimal, was more pronounced in E. esculentus than in P. miliaris and was due primarily to an increase in the internal P_{CO 2}, although there was an increase in the concentration of L-lactate in the coelomic fluid of E. esculentus. The coelomic fluid of both species was in a state of perfectly compensated respiratory acidosis. An increase in the concentration of divalent ions (Ca²⁺ and Mg²⁺) may be related to the dissolution of the test as a source of carbonate buffer.     

Quantifying the importance of regional and local filters for community trait structure in tropical and temperate zones

The influence of regional and local processes on community structure is a major focus of ecology. Classically, ecologists have used local-regional richness regressions to evaluate the role of local and regional processes in determining community structure, an approach that has numerous flaws. Here, we implemented a novel trait-based approach that treats local and regional influences as a continuum, rather than a dichotomy. Using hylid frogs (Hylidae), we compared trait dispersion among members of local species assemblages to the trait dispersion in the regional assemblage from which they were drawn. Similarly, we compared trait dispersion in the regional assemblages to dispersion in the continental species pool. We estimated the contributions of local and regional filters, and we compared their strength in temperate and tropical zones. We found that regional and local filters explained 80% of the total variation among local assemblages in community body size dispersion. Overall, regional filters reduced trait dispersion, and local filters increased it, a pattern driven by particularly strong antagonistic effects in temperate zones that reduced the realized total variation by more than 40%. In contrast, local and regional filters acted in concert in tropical regions. Patterns within the tropics did not differ from the random expectation based on a null model, but within the temperate zone, local community filtering was stronger than expected by chance. Furthermore, in temperate regions, antagonistic regional and local filtering masked from 76% to 90% of the total variation in trait dispersion. Together, these results suggest that there are fundamental differences in the scale and identity of the processes determining community structure in temperate and tropical regions.     

Heat waves,baby booms,and the destruction of kelp beds by sea urchins

Large populations of sea urchins, Strongylocentrotus droebachiensis (Müller), destroyed kelp beds along the Atlantic coast of Nova Scotia in the 1960's and 1970's. The origin of these large sea urchin populations is not understood. We have investigated the potential influence of variable growth and development of the planktonic larvae of sea urchins (in response to temperature and food abundance) on recruitment of benthic juveniles. The adult sea urchins were collected at Sandy Cove, Digby County, Nova Scotia, Canada, in December 1986. Temperature strongly affected larval size and the growth of the echinus rudiment within the range 3° to 9°C, and larvae grew most rapidly at 14°C. Food abundance had a smaller effect on larval growth, and these effects were apparent only at high temperature. Larvae fed the same concentration of two different algal food species grew and developed similarly. Correspondence between spring temperature variation and qualitative variation in sea urchin recruitment, as well as strong temperature effects on larval growth in culture, and the occurrence of a large, positive temperature anomaly in June 1960, all suggest that temperature effects on larval growth and development may have led to intense sea urchin recruitment in 1960 and the appearance of large adult populations 4 to 6 yr later. This result invites further research.     

Latitudinal variation in abundance of herbivorous fishes: a comparison of temperate and tropical reefs

The aim of the study was to provide comparable estimates of abundance of herbivorous reef fishes at temperate and tropical localities using a standardized methodology. Faunas of herbivorous fish were sampled on the rocky reefs of temperate northern New Zealand and on the coral reefs of the northern Great Barrier Reef (GBR), Australia, and the San Blas Archipelago in the Caribbean. A pilot study established the most appropriate habitat setting and the scale and magnitude of replication for the sampling program in temperate waters. Herbivorous fishes, including members of families endemic to the southern hemisphere (Odacidae and Aplodactylidae), were most abundant in turbulent, shallow water (0 to 6 m) and had patchy distributions within this habitat. A hierarchical sampling program using 10-min transect counts within the 0 to 6 m depth stratum examined abundance patterns at a range of spatial scales including mainland and island coasts, localities separated by up to 100 km and sites separated by up to 10 km. This program identified a characteristic fauna of seven species of herbivorous fishes with mean total abundances ranging from 23 to 30 individuals per 10-min transect. Species composition of the fauna varied between islands and coasts. A similar methodology was used to sample the major families of herbivorous fish in a number of sites in each of the tropical regions. These sampling programs revealed a fauna dominated by acanthurids and scarids in both the GBR and Caribbean localities. Estimates of abundance from these regions were similar, with a mean of 108 individuals recorded on the GBR and 129 per 10-min transect in the Caribbean. Species richness varied between each region, with 44 taxa recorded from the GBR and 11 from the Caribbean. Abundances of temperate water herbivores in New Zealand were found to be 75 to 80% lower than those recorded from shallow water habitats sampled on coral reefs. This was not related to species richness, since both New Zealand and the Caribbean locality had patterns of low richness. We suggest that the differences in abundance found by our study between temperate and tropical regions are not restricted to herbivorous fishes, but are representative of general latitudinal trends in reef fish faunas. Received: 4 November 1996 / Accepted: 15 December 1996     

The reproductive biology of echinothuriid and cidarid sea urchins from the deep sea (Rockall Trough,North-East Atlantic Ocean)

The reproductive biology of 5 species of echinothuriid (Phormosoma placenta, Calveriosoma hystrix, Araeosoma fenestrum, Sperosoma grimaldii and Hygrosoma petersii) and 2 species of cidarid (Cidaris cidaris and Poriocidaris purpurata) sea urchins from the deep sea (Rockall Trough) has been examined from samples collected during 1973–1983. In all species the gonads lie within the interambulacrum attached to aboral gonopores and when fully developed occupy most of the test not occupied by the gut or Aristotle's lantern. In all the species, initial oocyte development takes place along the germinal epithelium embedded in nutritive tissue. In all the echinothuriids and in Poriocidaris purpurata, the oocyte grows to ca. 200 to 450 m, at which stage vitellogenesis begins. Oocyte growth continues until a maximum egg size of 1 100 to 1 500 m is attained. In the echinothuriids, two types of nutritive tissue are found. In the carly stages of gametogenesis the oocyte is surrounded by well-structured periodic acid Schiff (PAS)-positive tissue. As the oocyte grows this tissue becomes vacuolated, suggesting that there is a transfer of nutriment to the developing oocyte. In Phormosoma placenta, unspawned oocytes are phagocytosed. There is no evidence of seasonality in any of the echinothuriid species or in Poriocidaris purpurata. Extrapolation with shallow-water echinothuriids suggests that larval development is lecithotrophic, omitting any planktotrophic phase. Of the species examined, only Cidaris cidaris has a reproductive strategy which produces a known larva, although the limited samples did not permit any determination of seasonality in this deep-sea population.     

Thermal tolerance of Strongylocentrotus purpuratus early life history stages: mortality, stress-induced gene expression and biogeographic patterns

In this study, we examined the differential thermal tolerance of Strongylocentrotus purpuratus early life history stages by comparing high temperature–induced mortality and the relative levels of the stress-induced gene, hsp70, between S. purpuratus embryos and larvae from adults collected throughout the species range. There was no significant difference between gastrulae and 4-arm plutei mortality from all sites examined. Furthermore, there was little variability in temperature tolerance across the biogeographic range as southern gastrulae and 4-arm plutei exhibited similar tolerances to northern individuals. Relative levels of hsp70 mRNA expression did not differ overall between the two developmental stages at each site. Across sites, all gastrulae and 4-arm plutei exhibited maximum hsp70 expression at approximately 25°C; however, the range of hsp70 expression was narrower in southern individuals, suggesting they are living closer to their upper thermal limit than northern individuals.     

Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei

Effects of acclimation to projected near-future ocean acidification (OA) conditions on physiology, reproduction and development were investigated in the tropical sea urchin Echinometra mathaei. Following 6 weeks in control or one of the three elevated pCO₂ (pH_NIST 7.5–8.1; pCO₂ ~485–1,770 μatm) conditions, adult urchins exhibited a slight decline of growth in low pH treatments and moderately reduced respiration at intermediate levels. At 7 weeks, gametes from adults were used to produce larvae that were reared in their respective parental treatments. To assess whether larvae from acclimated parents are more resilient to elevated pCO₂ than those not acclimated, larvae from control animals were also reared in the elevated pCO₂ treatments. There was no difference in female ‘spawnability’ and oocyte size between treatments, but male spawning ability was reduced in increased pCO₂ conditions. In elevated pCO₂ treatments, the percentage of normal larvae and larval size decreased in the progeny of control- and elevated pCO₂-acclimated parents, and arm asymmetry increased. Thus, acclimation of the parents did not make the progeny more resilient or sensitive to OA effects. Negative effects of increased pCO₂ on reproduction and development may impact on recruitment and population maintenance of this species.     

Tolerance to high temperatures and potential impact of sea warming on reef fishes of Gorgona Island (tropical eastern Pacific)

Knowledge of upper thermal-tolerance limits of marine organisms in the tropical eastern Pacific (TEP) is important because of the influence of phenomena such as El Niño and global warming, which increase sea temperature. Laboratory experiments were conducted to determine the critical thermal maximum (CTM) of reef fishes from the TEP. In 15 reef fishes of Gorgona Island (TEP) the CTM was between 34.7°C and 40.8°C. None of these CTMs was exceeded by sea temperature in the TEP during any of the strongest El Niño events in this century (32°C during El Niño 1982-1983 and 1997-1998), which indicates that all species studied here may tolerate El Niño maximum temperatures. In addition, the CTM of the least-tolerant species was 8°C above the current mean sea temperature in a wide range of latitudes in the TEP. This suggests that fishes live far from their upper thermal tolerance limits and that the current global-warming trend is still unlikely to be dangerous for these species. If sea temperature continues to increase at the current rate, in about a century sea temperature could exceed the thermal tolerance of some reef fishes and threaten them with extinction. Such risk, however, might occur sooner if the sea temperature during El Niño also increased in step with the global warming, but also because other processes involved in maintaining population, such as reproduction, can be affected at lower temperatures. The possible ability of reef fishes to adapt to increases in sea temperature is discussed.     

Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species

Ocean acidification, as a result of increased atmospheric CO₂, is predicted to lower the pH of seawater to between pH 7.6 and 7.8 over the next 100 years. The greatest changes are expected in polar waters. Our research aimed to examine how echinoid larvae are affected by lower pH, and if effects are more pronounced in polar species. We examined the effects of lowered pH on larvae from tropical (Tripneustes gratilla), temperate (Pseudechinus huttoni, Evechinus chloroticus), and a polar species (Sterechinus neumayeri) in a series of laboratory experiments. Larvae were reared in a range of lower pH seawater (pH 6.0, 6.5, 7.0, 7.5, 7.7, 7.8 and ambient), adjusted by bubbling CO₂ gas. The effect of pH on somatic and skeletal growth, calcification index, development and survival were quantified, while SEM examination of the larval skeleton provided information on the effects of seawater pH on the fine-scale skeletal morphology. Lowering pH resulted in a decrease in survival in all species, but only below pH 7.0. The size of larvae were reduced at lowered pH, but the external morphology (shape) was unaffected. Calcification of the larval skeleton was significantly reduced (13.8–36.9% lower) under lowered pH, with the exception of the Antarctic species, which showed no significant difference. SEM examination revealed a degradation of the larval skeletons of Pseudechinus and Evechinus when grown in reduced pH. Sterechinus and Tripneustes showed no apparent difference in the skeletal fine structure under lowered pH. The study confirms the need to look beyond mortality as a single endpoint when considering the effects of ocean acidification that may occur through the 21st century, and instead, look for a suite of more subtle changes, which may indirectly affect the functioning of larval stages.     

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.     

Maintenance of coelomic fluid pH in sea urchins exposed to elevated CO2: the role of body cavity epithelia and stereom dissolution

Experimental ocean acidification leads to a shift in resource allocation and to an increased [HCO₃ ^?] within the perivisceral coelomic fluid (PCF) in the Baltic green sea urchin Strongylocentrotus droebachiensis. We investigated putative mechanisms of this pH compensation reaction by evaluating epithelial barrier function and the magnitude of skeleton (stereom) dissolution. In addition, we measured ossicle growth and skeletal stability. Ussing chamber measurements revealed that the intestine formed a barrier for HCO₃ ^? and was selective for cation diffusion. In contrast, the peritoneal epithelium was leaky and only formed a barrier for macromolecules. The ossicles of 6 week high CO₂-acclimatised sea urchins revealed minor carbonate dissolution, reduced growth but unchanged stability. On the other hand, spines dissolved more severely and were more fragile following acclimatisation to high CO₂. Our results indicate that epithelia lining the PCF space contribute to its acid–base regulation. The intestine prevents HCO₃ ^? diffusion and thus buffer leakage. In contrast, the leaky peritoneal epithelium allows buffer generation via carbonate dissolution from the surrounding skeletal ossicles. Long-term extracellular acid–base balance must be mediated by active processes, as sea urchins can maintain relatively high extracellular [HCO₃ ^?]. The intestinal epithelia are good candidate tissues for this active net import of HCO₃ ^? into the PCF. Spines appear to be more vulnerable to ocean acidification which might significantly impact resistance to predation pressure and thus influence fitness of this keystone species.     

Day/night vertical distribution of euphausiids in the eastern tropical Pacific

Between March 23 and April 4, 1981, samples were taken in the eastern tropical Pacific. The day/night vertical distribution of euphausiid species and biomass are described and contrasted in detail on two eastern tropical Pacific stations, the DOME station, in a region of continuous upwelling and the BIOSTAT station, in a nonupwelling area. The effects of various biological parameters, such as temperature, salinity and oxygen concentrations on the distributions of the species are examined. The numbers of euphausiids m^-2 on both stations were highest during the day, indicating that avoidance of the sampler was not a problem. During the day the largest concentration of adult euphausiids was between 300 and 350 m whereas the juveniles were concentrated between 170 and 80 m on both stations. Very few individuals were found within the oxygen minimum layer, but low concentrations of some species were found below the oxygen minimum down to 1 000 m. At night the euphausiid concentration migrated upward into the mixed layer (20 to 30 m) at BIOSTAT and to the base of the mixed layer at the DOME. Significant differences in the night depths of the species were found on both stations. The oxygen minimum layer appeared to act as a barrier to the vertical distribution of all species. Only two species were found in water with an oxygen concentration of <0.1 ml O₂ l^-1. Twentyone species of euphausiids were found on the two stations but the adult population was dominated by only two or three species on both stations. The reproductive state of the species suggested that some species reproduced earlier on the DOME than on BIOSTAT. Analysis of the depth distribution by cluster analysis showed that the most abundant species occupied different depths during the night and day at BIOSTAT but the two most abundant species were concentrated at the same depth at the DOME station although portions of each species population occupied different pelagic zones.