Settlement and recruitment of sea urchins (Strongylocentrotus spp.) in a sea-urchin barren ground and a kelp bed: are populations regulated by settlement or post-settlement processes?

I sampled recruitment of very small sea urchins (Strongylocentrotus spp.) by using the anesthetic magnesium chloride to remove individuals from substrata collected in sea-urchin barren grounds (barrens) and kelp beds at Naples Reef near Santa Barbara, California, USA. Preliminary sampling found low numbers of newly settled individuals(<0.6 mm test diam) from April–July in 1984 and 1985, and in April, 1986. In early May, 1986, I found many newly settled seaurchins (0.3 to 0.6 mm, 5 to 17 d old), and I compared the densities of the cohort on several types of natural substrata in barrens and kelp-bed habitats. Newly settled individuals of both purple sea urchins (S. purpuratus) and red sea urchins (S. franciscanus) were present in similar, high densities (1 000 S. purpuratus m^-2) on foliose red algal turf, a dominant substratum ofthe kelp bed, and on crustose coralline algae, the dominant substratum of an adjacent barrens. Larvae of S. purpuratus reared and tested in the laboratory showed high rates of settlement on both red algal turf and on crustose coralline algae, but significantly lower rates on rock. Larvae also settled in response to a partiallypurified extract of coralline algae. The reduced settlement on natural rock surfaces relative to either algal treatment and the significant settlement in response to the extract of coralline algae indicate that larvae discriminate between natural substrata and probably respond to a settlement cue other than, or in addition to, a simple microbial (bacterial) film. The similar densities of young recruits of S. purpuratus on dominant substrata of barrens and kelp bed show that, at least in this case, differential settlement cannot explain the high densities of sea urchins in the barrens habitat. Movement between barrens and kelp bed is unlikely given the small sizes of the newly recruited sea urchins relative to the large distances often involved. Reduced post-settlement mortality of newly settled individuals in the barrens remains the most likely mechanism leading to the higher densities of sea urchins in barrens relative to kelp-bed habitats.     

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.     

Effects of food type and ration on reproductive maturation and growth of the sea urchin Strongylocentrotus droebachiensis

We investigated the effects of food quality and quantity on reproductive maturation and growth of juveniles of Strongylocentrotus droebachiensis (Müller) in a 22 month laboratory experiment in which we fed sea urchins four diets: (1) kelp (Laminaria spp.) for 6 d wk⁻¹ and mussel (Mytilus spp.) flesh for 1 d wk⁻¹ (KM); (2) kelp for 7 d wk⁻¹ (high ration, KH); (3) kelp for 1 d wk⁻¹ (low ration, KL) and (4) no food other than encrusting coralline algae (NF). At their first and second opportunity for reproduction, all sea urchins in the KM and KH treatments, and most in the KL treatment were reproductively mature, whereas all sea urchins in the NF treatment remained immature. Gonad index differed significantly among all fed treatments at first and second reproduction, and was highest in the KM and lowest in the KL treatment. Gonad index was similar in both sexes at first reproduction, but it was higher in females than in males at second reproduction. Diet had little or no effect on the relative abundance of spermatocytes, spermatozoa, or nutritive phagocytes in testes at first and second reproduction. In ovaries, nutritive phagocytes were significantly more abundant in females in the KM and KH treatments than in the KL treatment at first reproduction, and significantly more abundant in unfed (NF) than fed (KM, KH, KL) females at second reproduction. Mean oocyte size was similar in all fed females at first reproduction, but significantly larger in fed than unfed females at second reproduction. Mean ovum size was similar in all fed females in both reproductive periods. Increase in test diameter was greatest in the KM treatment and smallest in the KL treatment; sea urchins in the NF treatment decreased slightly in size. Survival was 95 to 100% in all fed sea urchins but significantly lower in unfed ones. The feeding rate on kelp was significantly greater in the KL than the KM and KH treatments. In the KM treatment, the feeding rate on kelp increased significantly over a 6 d period after mussel flesh was provided. Our results demonstrate that a diet of high food quality and quantity accelerates reproductive maturation and growth rate, and enhances gonad production and survival in juvenile and young adult S. droebachiensis. These findings contribute to our understanding of the reproductive ecology of S. droebachiensis in habitats with differing food supplies (e.g., kelp beds and barrens). Our results also can be used to improve aquacultural practices for sea urchins. Received: 3 June 1998 / Accepted: 2 February 1999     

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.     

Induction of larval settlement and metamorphosis of the sea urchin Strongylocentrotus intermedius by glycoglycerolipids from the green alga Ulvella lens

In aquaculture centers of the northern region of Japan, "Nami-ita" (waved polycarbonate plates), on which the green alga Ulvella lens Crouan frat. (Chaetophoraceae: Chaetophorales) was cultured, are used to promote larval settlement and metamorphosis of the sea urchin species Strongylocentrotus intermedius (A. Agassiz) and S. nudus (A. Agassiz). We investigated chemical inducer(s) for larval settlement and metamorphosis of these sea urchins with extracts of U. lens. Bioassay-guided separation of the methanol extract using a combination of column and thin-layer chromatography led to the isolation of several active compounds, the chemical structures of which were determined by spectral and chemical methods. These active compounds were identified as glycoglycerolipids, all comprising several molecular species: sulfoquinovosyl monoacylglycerols (SQMGs), sulfoquinovosyl diacylglycerols (SQDGs), monogalactosyl monoacylglycerols (MGMGs), monogalactosyl diacylglycerols (MGDGs), digalactosyl monoacylglycerols (DGMGs) and digalactosyl diacylglycerols (DGDGs). Among these glycolipids, SQMGs, MGMGs, MGDGs and DGMGs induced larval metamorphosis of the sea urchin S. intermedius. SQMGs and MGDGs induced larval metamorphosis at a concentration of 5 µg ml^-1, whereas SQDGs and DGDGs only induced larval settlement. These glycoglycerolipids are new congeners of chemical inducers to settlement and metamorphosis of planktonic larvae of sea urchins. The findings would provide a better understanding of larval settlement and metamorphosis in sea urchins.     

Fish predators and scavengers of the sea urchin Paracentrotus lividus in protected areas of the north-west Mediterranean Sea

Direct observations of predation on 436 individuals of the sea urchin Paracentrotus lividus (Lamarck) were carried out in infralittoral rocky bottoms (between 5 and 20 m deep) in three Mediterranean marine reserves. The predator guild was composed of six fish species, the sparids Diplodus sargus and D. vulgaris being the main predators, and the labrid Coris julis a major predator of juvenile sea urchins. Four species attempted but failed to open sea urchins. The scavenger guild was most rich in species, with 17 species observed. Predation was size-dependent; the size of predators increased with increasing size of the sea urchins. The presence of two feeding guilds is suggested, one composed of sparids (Diplodus spp.), able to kill juvenile and adult sea urchins, and the other composed of labrids (mainly C. julis), which feed on juvenile sea urchins. To avoid the extension of overgrazed, barren areas created by P. lividus populations, fisheries' regulations should focus on major sea-urchin predators, chiefly D. sargus, D. vulgaris and C. julis. Received: 23 April 1997 / Accepted: 30 May 1997     

Feeding aggregations of sea stars (<Emphasis Type="Italic">Asterias</Emphasis> spp. and <Emphasis Type="Italic">Henricia sanguinolenta</Emphasis>) associated with sea urchin (<Emphasis Type="Italic">Strongylocentrotus droebachiensis</Emphasis>) grazing fronts in Nova Scotia

Migrating feeding aggregations (or fronts) of sea urchins can dramatically alter subtidal seascapes by destructively grazing macrophytes. While direct effects of urchin fronts on macrophytes (particularly kelps) are well documented, indirect effects on associated fauna are largely unknown. Secondary aggregations of predators and scavengers form around fronts of Strongylocentrotus droebachiensis in Nova Scotia. We recorded mean densities of the sea stars Asterias spp. (mainly A. rubens) and Henricia sanguinolenta of up to 11.6 and 1.7 individuals 0.25 m⁻² along an urchin front over 1 year. For Asterias, mean density at the front was 7 and 15 times greater than in the kelp bed and adjacent barrens, respectively. There was strong concordance between locations of peak density of urchins and sea stars (Asterias r = 0.98; H. sanguinolenta r = 0.97) along transects across the kelp–barrens interface, indicating that sea star aggregations migrated along with the urchin front at rates of up to 2.5 m per month. Size–frequency distributions suggest that Asterias at the front were drawn from both the barrens (smaller individuals) and the kelp bed (larger individuals). These sea stars fed intensively on mussels on kelp holdfasts and in adjacent patches. Urchin grazing may precipitate aggregations of sea stars and other predators or scavengers by incidentally consuming or damaging mussels and other small invertebrates, and thereby releasing a strong odor cue. Consumption of protective holdfasts and turf algae by urchins could facilitate feeding by these consumers, which may obtain a substantial energy subsidy during destructive grazing events.     

Effect of sunlight intensity and albinism on the covering response of the Caribbean sea urchin<Emphasis Type="Italic"> Tripneustes ventricosus</Emphasis>

At Discovery Bay, Jamaica, Tripneustes ventricosus lives in beds of the turtle grass Thalassia testudinum. Especially during daylight hours, it covers its aboral surface with fragments of this plant and other objects. Normally pigmented, wild-type sea urchins covered themselves significantly less with Thalassia when sunlight was experimentally decreased to 66% or 32% ambient intensity. Consistent with this result, naturally occurring sea urchins exhibited significantly less covering at a deep (3.5 m) site than at a shallow (1 m) site, where light intensities at the bottom were 619 and 946 mol s^–1 m^–2, respectively. The graded covering response to light intensity suggests that covering is a defense against damaging solar radiation. Albino sea urchins covered themselves significantly more with Thalassia than wild-type sea urchins in both full and 66% sunlight. In addition, at the shallow site where they accounted for about 4% of the population, they showed significantly greater covering than wild-type urchins. The greater covering response of albino sea urchins suggests a greater susceptibility to solar radiation.Communicated by P. W. Sammarco, Chauvin     

Diel foraging patterns of the sea urchin Centrostephanus coronatus as a predator avoidance strategy

During the day, the diadematid sea urchin Centrostephanus coronatus occupies holes and crevices in shallow subtidal rocky substrata. Individuals emerge from these after sunset and forage on organisms attached to the surrounding rock surface. Each urchin travels <1 m from its shelter and returns to the same one before sunrise. The sheephead wrasse Pimelometopon pulchrum does not remove urchins from their shelters, but will attack and consume urchins placed in normal feeding locations during the daytime. The active periods of the sheephead and the urchin do not overlap; urchins begin foraging about 20 min after the diurnal sheephead retire in the evening and return to their shelters 1 to 2 h before sheephead resume feeding in the morning. We infer that the urchin's daytime crevice-dwelling and nocturnal foraging habits have evolved as a response to sheephead predation. Moreover, because shelters are limited in supply, shelter fidelity may have evolved to insure refuge from sheephead.     

Settlement, recruitment and potential predators and competitors of juvenile echinoderms in the rocky subtidal zone

Recruitment patterns of marine invertebrates are affected both by settlement and early post-settlement events. This study examined the settlement and recruitment patterns of echinoderms at three sites in the rocky subtidal zone of Bocabec Cove, Bay of Fundy, Canada using artificial turf collectors and quadrats on the natural substrate. Potential predators were quantified at two of the sites along transects and in 1-m² quadrats. Both potential predators and competitors were quantified in 0.0625-m² quadrats. Settlement varied across sites (1.5–3 km apart) and two years of sampling (2004, 2005). The site of most potential settlement differed for the three groups of echinoderms: sea urchins (Strongylocentrotus droebachiensis), sea stars (Asterias spp.) and sea cucumber (Psolus fabricii). Settlement densities on the artificial turf collectors tended to be greater than the densities of settlers on the natural substrate. On the natural substrate, the only significant difference between densities of juveniles over time was that newly settled sea stars were found in July and were not found the following October. Large lobsters and carnivorous worms were potential predators with densities that varied between sites. Potential competitors that differed in abundance between sites were herbivorous gastropods and conspecifics for sea urchins; and carnivorous worms for sea stars. This study suggests that patterns of recruitment are either set up by patterns of settlement or by events during the first few weeks/months on the benthic substrate for these echinoderms.     

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.     

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     

Growth and mortality of subtidal red sea urchins (Strongylocentrotus franciscanus) at San Nicolas Island,California, USA: problems with models

Red sea urchins, Strongylocentrotus franciscanus, were tagged with tetracycline in 1990 at subtidal sites off San Nicolas Island, California, USA. After one year in the field, the sea urchins were collected and growth increments were measured based on tetracycline marks, which indicated initial slow growth, a maximum rate, and finally a prolonged period of very slow growth. Small red sea urchins (4 cm diam) were estimated to be 3 to 4 yr old, which is much older than has previously been reported. It is estimated that about 12 yr would be required to attain 10 cm diam. Survival has previously been modeled assuming a constant rate. If the population of red sea urchins is assumed to be stable and stationary, annual survival rate was between 71 and 77% yr^-1. Census data for the two years of study have permitted annual survival to be estimated without assuming stable and stationary population structure. Under these conditions, annual survival rate was between 79 and 86% yr^-1. Analysis of transitions in the size distributions from 1990 to 1991 suggested that annual survival may have been sizespecific: 91% yr^-1 for individuals 1.1 to 4.0 cm diam, 82% yr^-1 for individuals 4.1 to 7.0 cm diam, and 63% yr^-1 for those of 7.1 to 10.0 cm diam. An alternative explanation to size-specific survival in our study is sizespecific immigration.     

Stability of sea urchin dominated barren grounds following destructive grazing of kelp in St. Margaret's Bay,Eastern Canada

Kelp regeneration was observed for the first time in St. Margaret's Bay, Nova Scotia, Canada in an area known to have been devoid of macroalgae for several years. The regeneration was destroyed by sea urchins within 10 months. Experimentally induced kelp regeneration met a similar fate under normal grazing pressure. At the lowest sea urchin biomass and density encountered re-establishment of mature kelp stands seems highly unlikely. The sea urchin population required to suppress kelp regeneration is fed by benthic microalgae. Diatoms and other pioneer algal community species were found in the guts of sea urchins. The mean standing crop of benthic microalgae was found to be, 2.2 g C m^-2 and production estimated as ca 15 g C m^-2yr^-1 at 8m depth. Most of the primary production of St. Margaret's Bay has been lost with the disappearing kelp populations.     

Crushing predation of the spiny star Marthasterias glacialis upon the sea urchin Paracentrotus lividus

Literature data report that only fish predators are able to crush sea urchin tests in Mediterranean rocky reefs. This experimental study showed that the spiny star Marthasterias glacialis is able to break Paracentrotus lividus tests and that the breaking event is more likely to occur for small-sized sea urchins than for big ones. Our results show that the role of M. glacialis in regulating P. lividus population density can be important in specific locations. They may have important implications, moreover, for the use of tethering techniques aimed at identifying predator types of sea urchins.     

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.     

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.     

Induction of metamorphosis of two species of sea urchin from Sea of Japan

The induction of metamorphosis in mature larvae by selected chemical compounds and natural substrata was investigated in two species of sea urchins from the Sea of Japan, Strongylocentrotus intermedius and Scaphechinus mirabilis. Glutamine in crystalline form was added directly to water containing mature larvae, and this compound, at a final concentration of 10 g ml^-1, was an inducer of metamorphosis in S. intermedius (100% activity) and S. mirabilis (50% activity). Gutamine, or its natural mimetic molecules, may be an active component of the exogenous cue that induces metamorphosis of S. intermedius larvae. This exogenous cue was produced by the epiphytic calcareous algae, Melobesia spp. that colonized the older sea grass Zostera marina. Glutamic acid was also used as an inducer of metamorphosis for S. intermedius and S. mirabilis larvae (50 to 60% activity), but it was toxic to the larvae.     

Detecting and quantifying male sea urchin spawning with time-integrated fertilization assays

There has been much modeling and experimentation on factors affecting fertilization success in free-spawning marine invertebrates, but for many species spawning has rarely been observed in nature, if at all, and then mostly qualitatively. Understanding the dynamics of spawning and fertilization is especially important for species, such as the green sea urchin, Strongylocentrotus droebachiensis (O.F. Müller), that have been widely depleted by harvesting. Time-integrated fertilization assays provide measures of sperm-availability adjacent to spawning populations for extended periods and with unprecedented temporal resolution. In such assays unfertilized eggs are held in baskets permeable to sperm and suspended in the water column as long as the eggs remain viable. In a consecutive series of 24- to 72-h assays the time course and spatial extent of sperm availability were measured near an aggregation of 250 sea urchins suspended in a cage at a field site in West Boothbay Harbor, Maine, USA. The assays were conducted in March and April, 2000, the spawning season of the green sea urchin. The distribution of embryonic stages within the assays revealed fine-scale temporal information on the timing of fertilization. The time series of multiple assays indicated that over a substantial portion of the spawning season there was an almost continuous low level of male spawning, a pattern consistent with a slow decline in gonad index observed in both male and female urchins. Fertilization rates averaged only 17% for the eggs in the basket nearest the spawning urchins (20 cm away), and the rates declined sharply over a distance of <1 m. Thus, despite the potential benefits of long egg life in integrating sperm supply over several days, the spatial effects on fertilization success were marked. Owing to the urchins' captivity and the lack of site replication, the generality of the observed spawning pattern must be confirmed. Nonetheless, the method lends itself to wider application among natural populations.     

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.