The diet of the Harlequin crab Lissocarcinus orbicularis,an obligate symbiont of sea cucumbers (holothuroids) belonging to the genera Thelenota,Bohadschia and Holothuria

The present paper characterizes, for the first time, the diet of the Harlequin crab Lissocarcinus orbicularis, an obligate symbiotic crab that associates with sea cucumbers (holothuroids) belonging to the genera Thelenota, Bohadschia and Holothuria. These tropical holothuroids host a rich symbiotic community in the Indo-West Pacific Ocean of which the Harlequin crab is the best known. The diet of L. orbicularis was characterized by analyzing the microscopic, molecular and isotopic signatures obtained from its gastric content. The presence of sea cucumber ossicles in the gastric mills of the crabs suggests that symbionts eat the superficial integument of their host and this was supported by the fact that Holothuroid DNA was detected in the stomach of L. orbicularis after DGGE and sequencing of the 18S rDNA gene. The stable isotopic δ¹³C and δ¹⁵N values of crab tissues were compared with diverse potential food sources including three holothuroids, three algae, one sea grass as well as the organic matter contained in the water column, in the sediment, and the second most abundant symbiont, the polychaete Gastrolepidia clavigera. The low δ¹⁵N values of crabs suggests that the crabs do not exclusively feed on sea cucumber tissue but assimilate diverse food sources such as sea grasses and organic matter contained in sediment that have similar δ¹³C values. There were no differences between the feeding of males and females but there was a positive correlation between the carapace length and the stable isotopic values indicating a shift of the food source as crabs grow larger.     

Best Dressed Test: A Study of the Covering Behavior of the Collector Urchin Tripneustes gratilla

Many sea urchin genera exhibit cryptic covering behaviors. One such behavior has been documented in the sea urchin Tripneustes gratilla, and previous studies have theorized that this behavior serves as protection from UV radiation. However, other hypotheses have been presented such as protection from predators or added weight to help T. gratilla resist strong currents. A field study was conducted in October-November 2015 in Moorea, French Polynesia to assess urchin covering behavior in natural habitats. The study found that urchins partially underneath rocks covered more, and with more algae, than urchins totally underneath rocks. To test if this behavior was driven by light intensity, a series of 30-minute experimental trials were run on 10 individuals in bright and dim conditions. Individuals were given red and clear plastic, and percent cover of each was recorded. These tests were repeated once fifty percent of spines had been removed from the urchin, in order to determine whether spine loss affects T. gratilla covering behavior. The study found that urchins had a distinct preference for cover that best protects them from UV radiation. Spine loss did not significantly affect urchin ability to cover, and urchins with removed spines still preferred opaque cover. Additionally, covering behavior was mapped onto a phylogeny of echinoderms to determine how it might have evolved. Understanding urchin covering behavior more fully is a step towards an understanding of the evolution of cryptic behavior across species.     

Estimation of foraging on the sea urchin <Emphasis Type="Italic">Strongylocentrotus droebachiensis</Emphasis> (Echinoidea: Echinoida) by the red king crab <Emphasis Type="Italic">Paralithodes camtschaticus</Emphasis> (Malacostraca: Decapoda) in coastal waters of the Barents Sea

A new method for the estimation of foraging on the sea urchin Strongylocentrotus droebachiensis (O.F. Müller, 1776) by the red king crab Paralithodes camtschaticus (Tilesius, 1815) is proposed. This method uses the reconstruction of the size, number, and biomass of eaten sea urchins, based on fragments of their teeth and tests from the crab’s digestive tract. Data obtained by this method suggest that in shallow waters of the Barents Sea (Kola Bay, Dal’nezelenetskaya Bay) adult, most often, female and immature crabs predominantly consume juvenile sea urchins. The weight of sea urchins daily eaten by one adult red king crab was 0.2–8.0% of its body weight for sexually mature crabs and 3.0–28.0% for immature specimens. Damage inflicted to the S. droebachiensis population as a result of the crab feeding activity was estimated to be at least 10% of the sea urchin biomass in Dal’nezelenetskaya Inlet and at least 30% in Kola Bay.     

Can multitrophic interactions and ocean warming influence large‐scale kelp recovery?

Ongoing changes along the northeastern Atlantic coastline provide an opportunity to explore the influence of climate change and multitrophic interactions on the recovery of kelp. Here, vast areas of sea urchin‐dominated barren grounds have shifted back to kelp forests, in parallel with changes in sea temperature and predator abundances. We have compiled data from studies covering more than 1,500‐km coastline in northern Norway. The dataset has been used to identify regional patterns in kelp recovery and sea urchin recruitment, and to relate these to abiotic and biotic factors, including structurally complex substrates functioning as refuge for sea urchins. The study area covers a latitudinal gradient of temperature and different levels of predator pressure from the edible crab (Cancer pagurus) and the red king crab (Paralithodes camtschaticus). The population development of these two sea urchin predators and a possible predator on crabs, the coastal cod (Gadus morhua), were analyzed. In the southernmost and warmest region, kelp forests recovery and sea urchin recruitment are mainly low, although sea urchins might also be locally abundant. Further north, sea urchin barrens still dominate, and juvenile sea urchin densities are high. In the northernmost and cold region, kelp forests are recovering, despite high recruitment and densities of sea urchins. Here, sea urchins were found only in refuge habitats, whereas kelp recovery occurred mainly on open bedrock. The ocean warming, the increase in the abundance of edible crab in the south, and the increase in invasive red king crab in the north may explain the observed changes in kelp recovery and sea urchin distribution. The expansion of both crab species coincided with a population decline in the top‐predator coastal cod. The role of key species (sea urchins, kelp, cod, and crabs) and processes involved in structuring the community are hypothesized in a conceptual model, and the knowledge behind the suggested links and interactions is explored.     

Sea Urchin Spines as a Model-System for Permeable, Light-Weight Ceramics with Graceful Failure Behavior. Part I. Mechanical Behavior of Sea Urchin Spines under Compression

The spines of pencil and lance urchins Heterocentrotus mammillatus and Phyllacanthus imperialis were studied as a modelof light-weight material with high impact resistance.The complex and variable skeleton construction ("stereom") of body andspines of sea urchins consists of highly porous Mg-bearing calcium carbonate.This basically brittle material with pronouncedsingle-crystal cleavage does not fracture by spontaneous catastrophic device failure but by graceful failure over the range of tensof millimeter of bulk compression instead.This was observed in bulk compression tests and blunt indentation experiments onregular,infiltrated and latex coated sea urchin spine segments.Microstructural characterization was carried out using X-raycomputer tomography,optical and scanning electron microscopy.The behavior is interpreted to result from the hierarchicstructure of sea urchin spines from the rnacroscale down to the nanoscale.Guidelines derived from this study see ceramics withlayered porosity as a possible biomimetic construction for appropriate applications.     

Why be cryptic? Choice of host urchin is not based on camouflage in the caridean shrimp Gnathophylloides mineri

The caridean shrimp Gnathophylloides mineri lives among the spines of various species of sea urchins. The shrimp has cryptic coloration that closely matches the coloration of the Caribbean urchin Tripneustes ventricosus. Despite this camouflage, in Jamaica, G. mineri is three times more abundant on the urchin Lytechinus variegatus than on T. ventricosus. L. variegatus exhibits more pronounced covering behavior than T. ventricosus. In laboratory choice experiments, the shrimp exhibited no preference between live, uncovered T. ventricosus or L. variegatus. Similarly, there was no preference between models (the tests, with spines attached, of hollowed out urchins) of T. ventricosus or L. variegatus without cover, or between models of T. ventricosus or L. variegatus with switched cover (i.e., each model was covered with the debris that had belonged to its partner when collected). There was, however, a significant preference for L. variegatus models with their natural covering over T. ventricosus with their natural covering. The shrimp may prefer L. variegatus with its extensive covering over T. ventricosus with extensive covering because the spines of the former are typically erect, as opposed to the spines of T. ventricosus, which usually lay flat across the test and would not give the shrimp much room to maneuver under the debris layer. Our study indicates that despite effective morphological and behavioral traits that render an organism highly cryptic, other, more effective, means of concealment may undermine the usefulness of this crypsis.     

Predation of the sea urchin Heliocidaris erythrogramma by rock lobsters (Jasus edwardsii) in no-take marine reserves

The formation of sea urchin ‘barrens’ on shallow temperate rocky reefs is well documented. However there has been much conjecture about the underlying mechanisms leading to sea urchin barrens, and relatively little experimentation to test these ideas critically. We conducted a series of manipulative experiments to determine whether predation mortality is an important mechanism structuring populations of the sea urchin Heliocidaris erythrogramma in Tasmania. Tethered juvenile and adult sea urchins experienced much higher rates of mortality inside no-take marine reserves where sea urchin predators were abundant compared to adjacent fished areas where predators were fewer. Mortality of tagged (but not tethered) sea urchins was also notably higher in marine reserves than in adjacent areas open to fishing. When a range of sizes of sea urchins was exposed to three sizes of rock lobsters in a caging experiment, juvenile sea urchins were eaten more frequently than larger sea urchins by all sizes of rock lobster, but only the largest rock lobsters (> 120 mm CL) were able to consume large adult sea urchins. Tagging (but not tethering) juvenile and adult sea urchins in two separate marine reserves indicated that adult sea urchins experience higher predation mortality than juveniles, probably because juveniles can shelter in cryptic microhabitat more effectively. In a field experiment in which exposure of sea urchins to rock lobster (Jasus edwardsii) and demersal reef fish predators was manipulated, rock lobsters were shown to be more important than fish as predators of adult sea urchins in a marine reserve. We conclude that predators, and particularly rock lobsters, exert significant predation mortality on H. erythrogramma in Tasmanian marine reserves, and that adult sea urchins are more vulnerable than smaller cryptic individuals. Fishing of rock lobsters is likely to reduce an important component of mortality in H. erythrogramma populations.     

Chemical composition of spines and tests of sea urchins

The skeleton of spines and tests of the species of sea urchins Strongylocentrotus intermedius, Mesocentrotus nudus, Scaphechinus mirabilis, and Echinocardium cordatum from the Sea of Japan is composed of a spongy stereom, consisting of calcite with a high content of magnesium. It was found that the tests and spines of the skeletons of sea urchins are composed of calcium–organic composite materials inlaid with other metals: Mg, Fe, Zn, and Rb. In the four species of sea urchins studied, the strength and other mechanical properties of the tests and spines differ and depend on the chemical composition and structural organization of their components. It was shown that the content of volatile substances correlates with their fragility or elasticity. It is revealed that the chemical composition of the tests of two species of the spherical sea urchins S. intermedius and M. nudus indicates significant differences between these two species of sea urchins.     

Utilization of purple and red sea urchins (Strongylocentrotus purpuratus Stimpson and S. franciscanus Agassiz) as food by the white sea urchin (Lytechinus anamesus Clark) in the field and laboratory

White sea urchins (Lytechinus anamesus Clark) attacked purple (Strongylocentrotus purpuratus Stimpson) and red (S. franciscanus Agassiz) sea urchins at Anacapa Island, California. Densities of white urchins were highest in the deep algal crust-dominated community where up to 6% of purple and 25% of red urchins were being attacked by white urchins. Up to 9% of Lytechinus anamesus in an area were actively eating stronglylocentrotids and usually, more than one white urchin was involved in the attack. In areas with low densities of white urchins, no strongylocentrotids were being attacked.After 36 h in the laboratory, there was no difference in the number of white urchins attacking injured or healthy purple urchins in each of the three experimental densities of white urchins. However, both injured and healthy urchins were attacked by more white urchins in high density. When given a choice between injured purple urchins or fresh kelp, white urchins overwhelmingly chose kelp. Data suggest that white urchins utilize other urchin species as an alternative source of food when more preferred food is absent, but will switch to preferred food should it become available.     

Responses of the black sea urchin Tetrapygus niger to its sea-star predators Heliaster helianthus and Meyenaster gelatinosus under field conditions

We ran field experiments to examine the responses of the black sea urchin Tetrapygus niger to predatory sea stars. Trials involving simulated attacks (one or several arms of a sea star being placed on top of half the urchin) showed that the urchin differentiated between the predatory sea stars, Heliaster helianthus and Meyenaster gelatinosus, and a non-predatory sea star, Stichaster striatus, and showed almost no response to a sea star mimic. We further compared the responses of the urchin to different threat levels presented by the two predatory sea stars. The highest threat level was a simulated attack, then mere contact, and subsequently sea stars being placed at different distances from the urchin. All urchins responded to simulated attacks and contact with both sea stars. The proportion responding decreased with distance and more rapidly in trials with H. helianthus (0% at a distance of 30 cm) than with M. gelatinosus (33% at a distance of 50 cm). At each of the threat levels where there was a response to both sea stars, the urchins responded more rapidly to M. gelatinosus than to H. helianthus. In a third experiment where a predatory sea star was added to a circular area (1-m diameter) in which either 4-8 or 11-19 undisturbed urchins were present, the urchins fled the area more rapidly when the added sea star was M. gelatinosus, but the rate of fleeing did not vary with density, as might occur if there was communication among urchins using alarm signals. Our observations suggest that M. gelatinosus presents a stronger predatory threat than H. helianthus. This corresponds to field observations showing that the urchins are more frequently consumed by M. gelatinosus. These are the first field experiments demonstrating distance chemodetection by a marine invertebrate under back-and-forth water flow from wave activity.     

Lissarca notorcadensis (Bivalvia: Philobryidae) living on Notocidaris sp. (Echinoidea: Cidaridae): Population dynamics in limited space

Summary Population dynamics of the epizoic bivalve Lissarca notorcadensis living on spines of cidaroid sea urchins in the Weddell Sea were investigated. Total production (somatic & gonad) of the suspension feeding bivalve ranged between 16.5 and 487.4 mg AFDM y^–1 per sea urchin. Annual sedimentation rates are not sufficient to maintain the production of the Lissarca sub-populations carried by the sea urchins, and resuspension of organic matter is most likely to be an important food source. The ratio of the number of freshly settled juveniles to the number of embryos brooded is between 0.054 and 0.207 and seems negatively related to the biomass already present, indicating intraspecific competition for space. Interspecific competition for space is caused by the strong preference of L. notorcadensis as well as other epizoa (colonial anthozoans and bryozoans) for the spines located on the aboral hemispere of the sea urchins.AWI Publication No. 572     

Morphological features and viability of Scrippsiella trochoidea cysts isolated from fecal pellets of the polychaete Capitella sp.

To investigate the impact of grazing by the polychaete Capitella sp. on the two cyst morphotypes of Scrippsiella trochoidea, the typical morphotype with short calcareous spines (spiny-type cyst) and artificially induced the transparent type without calcareous spines (naked-type cyst), we examined the morphological features and germination capability of the two cyst morphotypes isolated from fecal pellets of the polychaete Capitella sp. produced in a restricted habitat. The morphological destruction was observed in both spiny- and naked type cysts after passage through the gut of Capitella sp., and this seemed to occur rapidly for naked-type cysts. In addition, the germination of both spiny- and naked-type cysts isolated from fecal pellets on day 2 of harvesting was significantly reduced and subsequently completely abolished, in contrast to previous findings from ingestion studies. Our results indicate that continual grazing by Capitella sp. within a restricted habitat can compromise the survival of S. trochoidea cysts.     

Extraocular vision in the sea urchin Diadema setosum

In most organisms, specific structures are responsible for detecting light patterns and vision. Several species of sea urchins appear to have a diffuse photoreceptor system that enables them to detect light and in some cases objects. The presence of extraocular vision was investigated on a sea urchin common in northern Oman, Diadema setosum. Urchins from 8- to 10-m deep coral communities were used in controlled experiments that quantified the orientation response of the urchins to various visual cues: size, contrast and colour of circular targets simulating urchins’ outlines. Urchins responded to black discs down to 11° initial visual angle but not to smaller discs. The minimum grey-scale value triggering a response was between 50 and 37% black. Urchins responded to red targets but not to green or blue ones. An average angular distance between spines of 5.3° suggested a visual acuity of about 10.6°. D. setosum thus showed extraocular vision allowing them to detect objects of different sizes, contrasts and to some extent colour, supporting the hypothesis that the whole sea urchin’s body acts as a single large compound eye.     

Biological activity in extracts of ascidians (Tunicata, Ascidiacea) from the northeastern Brazilian coast

Ascidians are marine animals with a great ability to synthesize bioactive substances. This study examined the cytotoxic potential of 10 ascidians found in the coastal waters of Northeast Brazil. Samples of the species Eudistoma vannamei Millar, 1977, Eudistoma sp., Didemnum ligulum Monniot F., 1983, Didemnum psammatodes (Sluiter, 1895), Didemnum sp., Polysyncraton sp., Trididemnum sp., Cystodytes dellechiajei (Della Valle, 1877), Euherdmania sp., and an unidentified species belonging to the Holozoidae family were extracted in methanol 5:1 (v/w). The extracts were tested for cytotoxicity using the brine shrimp lethality assay, sea urchin egg development assay, hemolysis assay, and MTT assay using tumor cell lines. The extract of E. vannamei showed the highest toxicity in brine shrimp (LD₅₀=34.7 μg/ml) and in all tumor cell lines tested, with an IC₅₀ of <2 μg/ml for CEM, 11.2 μg/ml for HL-60, 23.8 μg/ml for B16, and 14.3 μg/ml for HCT-8. In sea urchin eggs, it inhibited the cell cycle progression mainly at the blastula stage (IC₅₀=74.8 μg/ml). The extract of Euherdmania sp. also exhibited some toxicity in these assays, but at a lower potency than that of E. vannamei. The extracts of D. psammatodes and Polysyncraton sp. showed a strong inhibition of the sea urchin egg cell cycle during both phases examined, first cleavage and blastula, with a possible action on the cell microfilament apparatus. The extract of D. ligulum showed selective toxicity toward HCT-8 cells (IC₅₀=35.3 μg/ml). The extract from the Holozoidae was the only one that possessed a hemolytic effect, with an IC₅₀ of 175.2 μg/ml. Further studies are necessary for a better characterization of the active principles of these extracts and a possible elucidation of the mechanisms of action.     

Effects of Light and Covering Behavior on PAX6 Expression in the Sea Urchin Strongylocentrotus intermedius

We studied the diel expression pattern of PAX6 (a structural gene that is commonly involved in the eye development and photoreception of eye forming animals) and the effects of light and covering behavior on PAX6 expression in the sea urchin Strongylocentrotus intermedius. We confirmed that aphotic condition significantly reduced covering behavior in S. intermedius. The diel expression pattern of PAX6 was significantly different in S. intermedius under photic and aphotic conditions. The gene expression of PAX6 significantly deceased in covered S. intermedius both under natural light and in darkness. The present finding provides valuable insight into the probable link between covering and PAX6 expression of sea urchins. Further studies are required to investigate the detailed expression network of light detection involved genes in order to fully reveal the molecular mechanism of the light-induced covering behavior of sea urchins.     

Microbial Composition and Genes for Key Metabolic Attributes in the Gut Digesta of Sea Urchins Lytechinus variegatus and Strongylocentrotus purpuratus Using Shotgun Metagenomics

This paper describes the microbial community composition and genes for key metabolic genes, particularly the nitrogen fixation of the mucous-enveloped gut digesta of green (Lytechinus variegatus) and purple (Strongylocentrotus purpuratus) sea urchins by using the shotgun metagenomics approach. Both green and purple urchins showed high relative abundances of Gammaproteobacteria at 30% and 60%, respectively. However, Alphaproteobacteria in the green urchins had higher relative abundances (20%) than the purple urchins (2%). At the genus level, Vibrio was dominant in both green (~9%) and purple (~10%) urchins, whereas Psychromonas was prevalent only in purple urchins (~24%). An enrichment of Roseobacter and Ruegeria was found in the green urchins, whereas purple urchins revealed a higher abundance of Shewanella, Photobacterium, and Bacteroides (q-value < 0.01). Analysis of key metabolic genes at the KEGG-Level-2 categories revealed genes for amino acids (~20%), nucleotides (~5%), cofactors and vitamins (~6%), energy (~5%), carbohydrates (~13%) metabolisms, and an abundance of genes for assimilatory nitrogen reduction pathway in both urchins. Overall, the results from this study revealed the differences in the microbial community and genes designated for the metabolic processes in the nutrient-rich sea urchin gut digesta, suggesting their likely importance to the host and their environment.     

A first report on the shrimp <Emphasis Type="Italic">Pontonia</Emphasis> sp. and other potential symbionts in the mantle cavity of the penshell <Emphasis Type="Italic">Pinna carnea</Emphasis> in the Dominican Republic

Examination of the mantle cavity of 310 penshells Pinna carnea, collected from seagrass beds in southwestern Dominican Republic, revealed the presence of four species from three phyla as potential symbionts. The shrimp Pontonia sp. was found in 178 penshells, the cardinalfish Astrapogon stellatus in 18, an anemone (order Actiniaria) in two, and a pea crab (family Pinnotheridae) in one. The penshell likely provides these organisms with a refuge from predators. It also provides nutrition for shrimp as they consumed food trapped in the mucus secreted by the penshell host. All of the cardinalfish, and 91% of the shrimp, were found in penshells measuring >150 mm in hinge length. At approximately 150 mm, the shells of P. carnea thicken and so flatten less when the valves are closed. As a result, larger penshells provide more mantle-cavity space for accommodating organisms. Shrimp and cardinalfish size increased with the size of the host penshell. The positive relationship between shrimp size and penshell size, a prevalence of male-female pairs of shrimp and other field observations, suggest that a long-term association exists between shrimp and penshells, and that the mating system of the shrimp involves social monogamy.     

不同实验生态环境对海刺猬遮蔽行为的影响

研究了较长时间生活在3种不同实验遮蔽条件下海刺猬(Glyptocidaris crenularis)的遮蔽行为特点。结果表明:不同生活环境下海刺猬都保持着遮蔽行为。生活在以贝壳作为遮蔽材料环境下(遮蔽组)和以砖块作为掩蔽材料环境下(掩蔽组)的海刺猬初次遮蔽耗时要显著短于生活在无遮蔽(或掩蔽)材料环境下(空白组)的海刺猬(N=3,P<0.05)。3组海刺猬用于遮蔽的贝壳总数和有遮蔽行为的海刺猬总数都呈现先增加后趋于平稳的趋势。掩蔽组有遮蔽行为的海刺猬总数要显著多于遮蔽组和空白组(P<0.05),后两者差异不显著。3组海刺猬用于遮蔽的贝壳总数差异不显著(P>0.05)。海刺猬遮蔽时对两种贝壳(菲律宾蛤仔和贻贝)存在显著的选择差异(P<0.05)。生活环境中一段时间内遮蔽物的缺失并不会使其失去这种行为,但是会在一定程度上影响该行为的强度。因此,光照很可能是海刺猬遮蔽行为的一个进化压力,该行为也许只是作为一种避光策略。海刺猬对遮蔽材料具有显著的选择性,这可能与遮蔽材料自身特征和海刺猬的生理状态相关。