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.     

Effects of body size and temperature on the metabolic rate of Penaeus monodon

Laboratory measurements of oxygen consumption were made on Penaeus monodon (Fabricius) from protozoea to adult stage at temperatures between 15° and 35°C. The logarithmic relationship between weight-specific respiration rate (WRt) and temperature (T) for two size groups, Protozoea 1 (PZ1) to Postlarva 1 (PL1) and PL to adult, are given as; WRt=10^{0.431+0.0146 (T)} (ml O₂ g^-1 h^-1) and WRt=10^{-0.948+0.0338 (T)} (ml O₂ g^-1 h^-1), respectively. Additionally, equations relating metabolic rate, temperature and size for the two size groups are; PZ1-PL1: log M=0.431+0.0146T+(1.25 (log TL)+0.579), and PL1-adult: log M=-0.948+0.0338T+(2.60(log CL)-0.683), where M=oxygen consumption in ml O₂ individual ^-1h^-1, T=temperature in °C, TL=total length in cm, and CL=carapace length in cm. Activation energies of 6 186.75 J for PZ1-PL1 and 14 066.62 J for PL-adults point to different metabolic pathways or to differences in the ratio between the metabolic pathways used.     

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.     

The association of N2-fixing bacteria with sea urchins

Dinitrogen fixation associated with bacteria in the gastrointestinal tract of sea urchins appears to be a widespread phenomenon: sea urchins from the tropics (Diadema antillarum, Echinometra lacunter, Tripneustes ventricosus), the temperature zone (Strongylocentrotus droebachiensis) and the arctic (S. droebachiensis) exhibited nitrogenase activity (C₂H₂ reduction). Pronounced seasonal variation was found in nitrogenase activity of temperate sea urchins feeding on kelp (Laminaria spp.) and eelgrass (Zostera marina). The mean monthly nitrogenase activity was inversely correlated with the nitrogen content of the sea urchin's food, which varied up to fivefold over the course of a year. The highest rate of nitrogenase activity recorded for a temperate sea urchin during the 14 month sampling period was 11.6g N fixed g wet wt^-1 d^-1, with a yearly mean activity of 1.36 g N fixed g wet wt^-1 d^-1. Studies with ¹⁵N confirmed the C₂H₂ reduction results and showed incorporation of microbially-fixed nitrogen into S. droebachiensis demonstrating that N₂ fixation can be a source of N for the sea urchin. Laboratory experiments indicated that part of the sea urchin's (S. droebachiensis) normal gastrointestinal microflora is responsible for the observed nitrogenase activity.     

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.     

Grazing by sea urchins at the margins of barren patches on Mediterranean rocky reefs

The role played by the urchins, Paracentrotus lividus and Arbacia lixula, in the formation and persistence of barren areas dominated by encrusting coralline macroalgae is yet to be fully elucidated. This study, carried out in the NW Mediterranean (43° 30′N, 10° 20′E) between February 2005 and April 2006, investigated how the loss or density decrease in one or both urchin species influences the recovery of erect macroalgal stands (dominated by filamentous forms) at the margins of barren areas. At a depth of 4–6 m, three barren patches were assigned to each of the following treatments: (1) control (natural densities of A. lixula and P. lividus); (2) 50 % of the natural density of A. lixula and natural density of P. lividus; (3) total removal of A. lixula and natural density of P. lividus; (4) 50 % of the natural density of P. lividus and natural density of A. lixula; (5) total removal of P. lividus and natural density of A. lixula; (6) 50 % of the natural densities of both A. lixula and P. lividus; (7) total removal of both A. lixula and P. lividus. The effects of the herbivore treatments were evaluated either in the presence or the absence of encrusting corallines. The partial or total removal of A. lixula, P. lividus or both favored the proliferation of filamentous macroalgae at the margins of barren patches. The presence of encrusting corallines reduced the development of these macroalgae. The results of this study suggest that a moderate decrease in the density of just one of the two species can decrease the ability of the herbivore assemblage to control the proliferation of filamentous macroalgae at the margins of barren patches. The extent of barren areas appears, therefore, to be regulated by the outcome of density-dependent interactions between the two species of sea urchins.     

Waterborne cues from crabs induce thicker skeletons, smaller gonads and size-specific changes in growth rate in sea urchins

Indirect predator-induced effects on growth, morphology and reproduction have been extensively studied in marine invertebrates but usually without consideration of size-specific effects and not at all in post-metamorphic echinoids. Urchins are an unusually good system, in which, to study size effects because individuals of various ages within one species span four orders of magnitude in weight while retaining a nearly isometric morphology. We tracked growth of urchins, Strongylocentrotus droebachiensis (0.013–161.385 g), in the presence or absence of waterborne cues from predatory Jonah crabs, Cancer borealis. We ran experiments at ambient temperatures, once for 4 weeks during summer and again, with a second set of urchins, for 22 weeks over winter. We used a scaled, cube-root transformation of weight for measuring size more precisely and for equalizing variance across sizes. Growth rate of the smallest urchins (summer: <17 mm diameter; winter: <7 mm diameter) decreased by 40–42% in response to crab cues. In contrast, growth rate of larger urchins was unaffected in the summer and increased in response to crab scent by 7% in the winter. At the end of the 22-week experiment, additional gonadal and skeletal variables were measured. Cue-exposed urchins developed heavier, thicker skeletons and smaller gonads, but no differences in spine length or jaw size. The differences depended on urchin size, suggesting that there are size-specific shifts in gonadal and somatic investment in urchins.     

Expansion of a central California kelp forest following the mass mortality of sea urchins

The mass mortality by disease of a localized population of sea urchins, Strongylocencrotus franciscanus, on the seaward side of a kelp forest was followed by the rapid seaward expansion of 4 species of brown algae, Macrocystis pyrifera, Laminaria dentigera, Pterygophora california, and to a lesser extent, Nereocystis leutkeana. One other brown alga, Cystoseira osmundacea, failed to become established in the newly available area. Competition among M. pyrifera, L. dentigera, P. californica, and N. Leutkeana apparently was severe, and within 1 year after the demise of the sea urchins, M. pyrifera formed a dense, nearly monospecific stand. Experimental removal of M. pyrifera demonstrated that the canopy of these plants limited light penetration to levels below that necessary for the growth and survival of other brown and red algae.     

Comparative sensitivity of various developmental stages of sea urchins to some chemicals

The sensitivity to some chemical agents was examined comparatively at sperm, fertilization, cleavage, blastula, gastrula, pluteus and metamorphosis stages of a sand dollar from Japanese waters (Peronella japonica) and a sea urchin from the Pacific coast of Australia (Heliocidaris erythrogramma). These agents included Cu sulphate, ABS and NH₃ chloride. Responses observed included departures from control rates of fertilization and developmental reduction at the attainment of first cleavage, gastrula, pluteus or metamorphosis. Developmental anomalies were noted at the fertilization, 2-cell, gastrula, pluteus and metamorphosis stages. Using minimum effective concentrations of the 3 chemicals at various developmental stages of P. japonica, it was found that sensitivity to chemicals varies from fertilization to metamorphosis. It seems that sperm activity is the most sensitive, and that fertilization and gastrulation are more sensitive than first cleavage, blastulation and pluteus formation. H. erythrogramma seems to show nearly the same responses to Cu, but is more sensitive at metamorphosis.Experiments conducted at the Seto Marine Biological Laboratory, Wakayama Prefecture, JapanExperiments conducted at School of Biological Sciences, the University of Sydney, Sydney, N.S.W., AustraliaContributions from the Seto Marine Biological Laboratory, No. 664     

The effects of predator abundance and habitat structural complexity on survival of juvenile sea urchins

We studied the effect of the abundance of predatory fishes and structural complexity of algal assemblages on the survival of juveniles of the sea urchin Paracentrotus lividus on Mediterranean infralittoral rocky bottoms. Post-settlement juveniles (2–10 mm) were placed on four distinct natural substrates with increasing structural complexity (coralline barren, algal turf, erect fleshy algal assemblages and small crevices) inside and outside the Medes Islands Marine Reserve. Predation on these sea urchins increased at greater abundance of predatory fishes, and decreased with greater structural complexity. The refuge provided by structural complexity, however, decreased with increasing size of sea urchin recruits. Predation on the smallest post-settlers was carried out almost exclusively by small fishes (<20 cm), mainly the labrid Coris julis, while the dominant predator of larger juveniles was the sparid Diplodus sargus. Our results demonstrate the cascading effects caused by the prohibition of fishing in marine reserves, and highlight the potential role of small predatory fishes in the control of sea urchin populations.Communicated by O. Kinne, Oldendorf/Luhe     

Effect of temperature and temperature adaptation on calcification rate in the hermatypic coral Pocillopora damicornis

Using ⁴⁵Ca incorporation into the coral skeleton as a measure of calcification rate, the effect of temperature on clacification rate was studied in the hermatypic coral Pocillopora damicornis. Both immediate and long-term (adaptation) effects were investigated. Temperature has a marked effect on rate — an effect that varies depending on the temperature history of the coral (i.e., temperature adaptation occurs). P. damicornis showed both 27° and 31°C temperature optima, one or the other being dominant depending on the natural water temperature to which the coral was adapted. The two optimum temperatures may indicate two isoenzymes or two alternate metabolic pathways involved in the calcification process.     

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.     

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.     

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.     

The effects of temperature and pressure acclimation on the temperature and pressure tolerance of the shallow-water shrimp Palaemonetes varians

Anthropogenic effects on marine ecosystems (e.g. hypoxia, warming) at and beyond continental margins are assumed to affect physiological and biochemical boundaries to species’ distributions, potentially leading to habitat contraction across depth. Whether or not shallow-water benthic invertebrates are capable of undergoing depth-related migrations in response to such perturbations remains largely unknown. The few studies available have focused solely on whether colonisation of deep waters may be ongoing and on the ability of shallow-water species to tolerate low temperatures and high hydrostatic pressures: two physical parameters, which are thought to limit the depth range of a species. Those studies did not consider the effects of acclimation to low temperature and, especially, acclimation to high hydrostatic pressure on pressure tolerance. We demonstrate that acclimation to both low temperature (5 °C) and to high hydrostatic pressure (10 MPa) increases the pressure tolerance within the shallow-water shrimp Palaemonetes varians. Previous studies have demonstrated the impressive temperature and pressure tolerance of this shallow-water shrimp. Here, we provide evidence that a shallow-water species may acclimate to low temperature and high pressure and show greater pressure tolerance, suggesting that shallow-water organisms may be able to rapidly—and potentially stepwise—acclimate to the low temperature and high pressure conditions typical of the deep sea. These findings are of importance for understanding phylogenetic development from shallow- to deep-water species and the processes behind past, present and future bathymetric range shifts in species.     

Some new data on skin-digestion and absorption in urchins and sea stars (Asterias and Henricia)

An adult Psammechinus miliaris, and another specimen 8 mm in diameter were both fed apically by deposition of a protein-powder extracted from a heavily ¹⁴C-tagged urchin. The organs of the former were counted and the latter was totally sectioned and autoradiographed. The gut was more labelled than expected after an apical meal. This could be explained by a pumping of some nutritive powder into the gut, the bright marking of the superficial tissues being obviously due to direct uptake. The localized proteolysis produced by a podial disc of P. miliaris on a black gelatin-film may be due to the secretion of special cell-masses just underlying the calcareous plates of the disc. Extracts from mucus, small spines and dorsal podia from the anterior furrow of Echinocardium cordatum produce a conspicuous digestion of Remazol-brilliant blue hidepowder in vitro. Several in vivo tests with artificial substrates suggest the existence of a trypsin-like enzyme and not chymiotrypsin in the mucus. Fresh frozen sections in podia of Asterias rubens treated with A.S. naphthol-propionate showed that special cells, scattered in the connective tissue, gave a dark-red stain. Strains of red granules issued by them found their way to the surface of the disc between the columnar epithelial cells. These chimiotrypsin-positive cells and their products seem identical to those seen by Chaet and Philpot (1964) in A. forbesi. These authors did not suspect their digestive function. The nutrition of Henricia sanguinolenta through the body wall was tested either with radioactive diatoms or ¹⁴C-labelled amino acids in sea water selectively offered to one or two arms. Both countings and autoradiographs demonstrated the importance of skin-digestion and absorption, especially in the ambulacra. The absorbed nutrients reach the muscle layer, not only the epiderm as mentioned in Ferguson's (1967) esperiments.     

Some effects of temperature on the growth and metabolic rate of juvenile blue crabs,Callinectes sapidus,in the laboratory

Juvenile blue crabs, Callinectes sapidus Rathbun, were grown in the laboratory at different temperatures, and metabolic-rate determinations were made. Growth is shown to be dependent upon temperature. Crabs kept at high temperatures (34° and 27°C) grow faster than those kept at lower temperatures (13°, 15°, and 20°C). Increase in size per molt is less at higher temperatures than at lower ones. Mortality is directly proportional to temperature between 13° and 34°C and is very high during ecdysis at elevated temperatures. Metabolic rate increases with temperature, but various degrees of acclimation are seen after 4 weeks exposure. No acclimation of general activity to temperature was found. The findings are applied theoretically to crabs living in the region of heated discharge canals of electrical generators: the motile blue crab could extend its growing season without decreasing size at maturity by active selection of thermal surroundings.In part based on a thesis submitted in partial fulfillment of the requirements for the Degree of Master of Science at the University of Florida, USA.     

Thermal tolerance of early development in tropical and temperate sea urchins: inferences for the tropicalization of eastern Australia

The thermal envelope of development to the larval stage of two echinoids from eastern Australia was characterized to determine whether they fill their potential latitudinal ranges as indicated by tolerance limits. The tropical sand dollar, Arachnoides placenta, a species that is not known to have shifted its range, was investigated in Townsville, northern Australia (19°20′S, 146°77′E), during its autumn spawning season (May 2012). The subtropical/temperate sea urchin, Centrostephanus rodgersii, a species that has undergone poleward range expansion, was investigated in Sydney, southern Australia (33°58′S, 151°14′E), during its winter spawning season (August 2012). The thermal tolerance of development was determined in embryos and larvae reared at twelve temperatures. For A. placenta, the ambient water temperature near Townsville and experimental control were 24 °C and treatments ranged from 14 to 37 °C. For C. rodgersii, ambient Sydney water temperature and experimental control were 17 °C, and the treatment range was 9–31 °C. A. placenta had a broader developmental thermal envelope (14 °C range 17–31 °C) than C. rodgersii (9 °C range 13–22 °C). Both species developed successfully at temperatures well below ambient, suggesting that cooler water is not a barrier to poleward migration for either species. Both species presently live near the upper thermal limits for larval development, and future ocean warming could lead to contractions of their northern range limits. This study provides insights into the factors influencing the realized and potential distribution of planktonic life stages and changes to adult distribution in response to global change.     

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.     

Movement and feeding activity of red sea urchins (Strongylocentrotus franciscanus) adjacent to a kelp forest

Movement and feeding were studied in a population of red sea urchins, Strongylocentrotus franciscanus (Agassiz, 1863), found within and immediately seaward of a kelp forest offshore from Santa Cruz, California, USA. Mean sea urchin movements varied from 7.5 cm/day inside the kelp forest to over 50 cm/day at 15 and 100 m outside the kelp forest. The percentage of sea urchins feeding decreased from 66% inside the kelp forest to 16 and 15% at 15 and 100 m outside the kelp forest. These data indicate that movement by these sea urchins is a response to a low food supply.