Biochemical investigation of two responses involved in the feeding behaviour of Acanthaster planci (L.). II. Isolation and characterization of chemical stimuli

Feeding behaviour is induced in the crown-of-thorns starfish, Acanthaster planet (L.), by two kinds of chemical stimulus originating in coral. One is macromolecular, and the other of low molecular weight, largely accounted for by small peptides and amino acids.It is found that, under experimental conditions, starfish rapidly habituate to a chemical stimulus which at first strongly induces feeding behaviour.The pronounced withdrawal response which occurs when a crude extract of coral is applied to the starfish (a response apparently identical with that evoked by contact with live coral) is caused by a component which corresponds closely in chromatographie behaviour with proline. Proline itself produces the response, but is present at too low a concentration in coral to account for the observed activity.     

Biochemical investigation of two responses involved in the feeding behaviour of Acanthaster planci (L.). III. Food preferences

The arm-withdrawal and settlement responses associated with feeding in Acanthaster planet (L.) are elicited at differing intensities by various species of coral and by extracts of these corals. There is no clear correlation between the strengths of the two responses. The preferences shown by A. planci for certain species of whole coral depend on the previous dietary experience of the starfish, and repeated presentation of an unfamiliar coral may increase its acceptability as food.     

Homing behaviour by destructive crown-of-thorns starfish is triggered by local availability of coral prey

Corallivorous crown-of-thorns starfishes (Acanthaster spp.) can decimate coral assemblages on Indo-Pacific coral reefs during population outbreaks. While initial drivers of population irruptions leading to outbreaks remain largely unknown, subsequent dispersal of outbreaks appears coincident with depletion of coral prey. Here, we used in situ time-lapse photography to characterize movement of the Pacific crown-of-thorns starfish (Acanthaster cf. solaris) in the northern and southern Great Barrier Reef in 2015, during the fourth recorded population outbreak of the starfish, but prior to widespread coral bleaching. Daily tracking of 58 individuals over a total of 1117 h revealed all starfish to move a minimum of 0.52 m, with around half of all tracked starfish showing negligible daily displacement (less than 1 m day⁻¹), ranging up to a maximum of 19 m day⁻¹. Movement was primarily nocturnal and daily displacement varied spatially with variation in local availability of Acropora spp., which is the preferred coral prey. Two distinct behavioural modes emerged: (i) homing movement, whereby tracked paths (as tested against a random-walk-model) involved short displacement distances following distinct ‘outward'' movement to Acropora prey (typically displaying ‘feeding scars'') and ‘homebound'' movement to nearby shelter; versus (ii) roaming movement, whereby individuals showed directional movement beyond initial tracking positions without return. Logistic modelling revealed more than half of all tracked starfish demonstrated homing when local abundance (percentage cover) of preferred Acropora coral prey was greater than 33%. Our results reveal facultative homing by Acanthaster with the prey-dependent behavioural switch to roaming forays providing a mechanism explaining localized aggregations and diffusion of these population irruptions as prey is locally depleted.     

Plant-growth regulators from common starfish (<Emphasis Type="Italic">Asterias amurensis</Emphasis> Lütken) waste

Starfish waste has been shown to be an effective compost material not only in the promotion of plant growth but also in terms of having insecticidal activity. In the present study, plant growth regulation by chemicals from starfish was examined. The aqueous fraction from a hot water extract of the starfish Asterias amurensis Lütken showed plant-growth activity, while the aqueous fraction from a methanol extract inhibited growth of Brassica campestris. The lipophilic fraction from the methanol extract also exhibited a plant growth-promoting effect. The active components from each extract were identified. Asterubine from the hot water extract promoted plant growth. A ceramide from the lipophilic fraction showed root growth promoting effect, and three glucocerebrosides had promotive effects on the entire plant. Asterosaponins were identified as the main growth inhibitors in the aqueous fraction of the methanol extract. These active compounds from starfish waste could be analyzed as potential plant growth regulators in agricultural applications in the future.     

Acanthaster planci is a major cause of coral mortality in Indonesia

The corallivorous crown-of-thorns starfish (COTS), Acanthaster planci, is recognised as a major cause of coral reef degradation throughout much of the Pacific Ocean. However, the effects of COTS on the high diversity reefs in Indonesia have been largely overlooked. In 2007, high densities of COTS were observed in two regions of Indonesia: Aceh and Halmahera. Densities of COTS ranged from 0 to 52 starfish 2,000 m² across 24 sites in Aceh and from 0 to 18 starfish 2,000 m² at 10 sites in Halmahera. Mortality rates of Acropora spp. were very high at affected sites: over 50 % of colonies had been killed at seven of the 16 affected sites. A review of historical sources going back to 1969 suggests that COTS have damaged many reefs throughout Indonesia, including much activity within the Indonesian section of the Coral Triangle. Furthermore, the data suggest that COTS activity has increased rapidly since 2000. Very little of this activity has been reported in the primary literature, and there is a general lack of awareness in Indonesia of COTS as a potential cause of reef degradation. This lack of awareness, combined with limited monitoring efforts, means that damage caused by COTS is often attributed to other causes, such as destructive fishing, bleaching or tsunami. COTS are clearly a major source of coral mortality in Indonesia of which scientists and government need to be more cognizant.     

Factors affecting the behaviour of crown-of-thorns starfish (Acanthaster planci L.) on the Great Barrier Reef:: 1: Patterns of activity

The feeding, moving and cryptic behaviours of 5749 crown-of-thorns starfish, Acanthaster planci (L.), were studied on 15 reefs of the Great Barrier Reef between June 1986 and December 1987. Log-linear analyses of field data showed that these behaviours were influenced by complex interactions between a number of important physical and biological factors including the size of starfish, their depth and physical condition, time of day, and substratum type. For most of these factors, the patterns of behaviour were shown to be consistent across reefs. Irrespective of their size, starfish spent on average about 45% of their time feeding. However, there were strong diurnal effects with smaller starfish (<20 cm) strongly favouring nocturnal feeding. For larger starfish (>40 cm) this pattern was reversed, though the diurnal effects were not as strong. Diurnal variation was greater at shallower depths (<3 m). Larger starfish spent more time moving (∼20%), particularly during the day, compared to smaller starfish (∼5%), with the latter moving mainly at night. Motion increased with depth for all starfish. The density and degree of aggregation of starfish had no effect on behaviour. The cryptic behaviour of starfish decreased with size, from ∼60% for small starfish to less than 10% for large starfish. For starfish <30 cm in size, there were strong diurnal effects on cryptic behaviour, with smaller starfish being almost exclusively cryptic during the day. Cryptic behaviour was also influenced by the condition of starfish. Those in poor condition were 5 times more likely to be moving than those in good condition. Cryptic starfish were 10 times more likely to be in good condition than non-cryptic starfish. This may partly explain the relatively rapid breakdown in starfish aggregations which has been observed at the ends of outbreaks.     

Crown-of-thorns starfish have true image forming vision

Background

Photoreceptors have evolved numerous times giving organisms the ability to detect light and respond to specific visual stimuli. Studies into the visual abilities of the Asteroidea (Echinodermata) have recently shown that species within this class have a more developed visual sense than previously thought and it has been demonstrated that starfish use visual information for orientation within their habitat. Whereas image forming eyes have been suggested for starfish, direct experimental proof of true spatial vision has not yet been obtained.

Results

The behavioural response of the coral reef inhabiting crown-of-thorns starfish (Acanthaster planci) was tested in controlled aquarium experiments using an array of stimuli to examine their visual performance. We presented starfish with various black-and-white shapes against a mid-intensity grey background, designed such that the animals would need to possess true spatial vision to detect these shapes. Starfish responded to black-and-white rectangles, but no directional response was found to black-and-white circles, despite equal areas of black and white. Additionally, we confirmed that starfish were attracted to black circles on a white background when the visual angle is larger than 14°. When changing the grey tone of the largest circle from black to white, we found responses to contrasts of 0.5 and up. The starfish were attracted to the dark area’s of the visual stimuli and were found to be both attracted and repelled by the visual targets.

Conclusions

For crown-of-thorns starfish, visual cues are essential for close range orientation towards objects, such as coral boulders, in the wild. These visually guided behaviours can be replicated in aquarium conditions. Our observation that crown-of-thorns starfish respond to black-and-white shapes on a mid-intensity grey background is the first direct proof of true spatial vision in starfish and in the phylum Echinodermata.

     

Generality of the action of various maturation-promoting factors

It has been known in amphibians and starfishes that a cytoplasmic factor called maturation-promoting factor (MPF), produced in maturing oocytes under the influence of the maturation-inducing hormones, can induce germinal vesicle breakdown (GVBD) and the subsequent process of meiotic maturation. The present study revealed that injection of cytoplasm of maturing starfish oocytes (starfish MPF) into immature sea cucumber oocytes brought about maturation of the recipients. Amphibian MPF obtained from mature oocytes of Xenopus laevis or Bufo bufo was found to induce maturation of starfish oocytes following injection. Cytoplasm taken from cleaving starfish blastomeres induced maturation when injected into immature starfish oocytes. The maturation-inducing activity of cytoplasm of starfish blastomeres changed along with the mitotic cell cycle during 1- to 4-cell stages so far tested and reached a peak just before cleaving. Furthermore, an extract of mammalian cultured cells, CHO or V-79, synchronized in M phase, induced GVBD in starfish oocytes following injection, whereas S phase extract had little activity. These facts suggest that MPF generally brings about nuclear membrane breakdown in both meiosis and mitosis, and that the nature of MPF is very similar among vertebrates and invertebrates.     

Calmodulin in starfish oocytes. I. Calmodulin antagonists inhibit meiosis reinitiation

A heat-stable factor has been found in starfish (Patiria miniata and Marthasterias glacialis) oocytes that activates two calmodulin-dependent enzymes: bovine brain phosphodiesterase (10-fold increase) and sea urchin egg NAD-kinase (10- to 50-fold increase). The dose-response curves for activation of these enzymes were found to be parallel for the starfish egg extract and pure mammalian brain calmodulin. The active factor was purified by chromatography on DE 52 cellulose to which it remained bound and was eluted by 0.225 M ammonium sulfate. Active fractions were pooled, dialyzed, and run on a polyacrylamide gel. The starfish active factor comigrated with pure bovine brain calmodulin. A radioimmunoassay was performed on the purified factor; it cross-reacted with antibodies against pure calmodulin. That calmodulin may play a role in hormonally induced maturation of starfish oocytes is suggested by the fact that two calmodulin antagonists (trifluoperazine and vinblastine), which are also inhibitors of NAD-kinase, were found to block 1-methyladenine-induced oocyte maturation. The inhibition could be reversed by increasing the hormone concentration. Oocytes were sensitive to trifluoperazine only during the hormone-dependent period.     

Specialization in habitat use by coral reef damselfishes and their susceptibility to habitat loss

While it is generally assumed that specialist species are more vulnerable to disturbance compared with generalist counterparts, this has rarely been tested in coastal marine ecosystems, which are increasingly subject to a wide range of natural and anthropogenic disturbances. Habitat specialists are expected to be more vulnerable to habitat loss because habitat availability exerts a greater limitation on population size, but it is also possible that specialist species may escape effects of disturbance if they use habitats that are generally resilient to disturbance. This study quantified specificity in use of different coral species by six coral‐dwelling damselfishes (Chromis viridis, C. atripectoralis, Dascyllus aruanus, D. reticulatus, Pomacentrus moluccensis, and P. amboinensis) and related habitat specialization to proportional declines in their abundance following habitat degradation caused by outbreaks of the coral eating starfish, Acanthaster planci. The coral species preferred by most coral‐dwelling damselfishes (e.g., Pocillopora damicornis) were frequently consumed by coral eating crown‐of‐thorns starfish, such that highly specialized damselfishes were disproportionately affected by coral depletion, despite using a narrower range of different coral species. Vulnerability of damselfishes to this disturbance was strongly correlated with both their reliance on corals and their degree of habitat specialization. Ongoing disturbances to coral reef ecosystems are expected, therefore, to lead to fundamental shifts in the community structure of fish communities where generalists are favored over highly specialist species.     

Prey selection and the impact of the starfish Marthasterias glacialis (L.) and other predators on the mussel Choromytilus Meridionalis (Krauss)

The diet of the starfish, Marthasterias glacialis (L.), consists of a variety of mollusc species, as well as ascidians and barnacles. Starfish densities are maximal where mussels, Choromytilus meridionalis (Krauss), are abundant and in such areas mussels form the bulk of the diet. Laboratory feeding experiments indicate that Marthasterias glacialis select mussels of particular sizes and that the length of prey taken is an increasing function of predator arm length. The time taken to consume each mussel is determined by the ratio of shell length to starfish size. The number of mussels consumed per day increases only slightly with starfish size, but because the prey taken increase in size, energy consumption is maintained at a relatively consistent 1% of predator body energy per day. Using prey selection and feeding rate data for different sized starfish, predictive three dimensional predation surfaces are developed for a natural starfish population feeding on either one or two cohort Choromytilus meridionalis populations. The models indicate that predatory effort should be concentrated on the smallest mussels when a single adult cohort is present, but on recruiting mussels just above the minimum prey size limit where two cohorts are present. Other major predators of mussels, the rock lobster, Jasus lalandii (Milne Edwards), and the whelk, Natica tecta Anton, appear to select similar size-ranges of prey to starfish, despite their differing body forms and feeding methods. Since the juveniles of all three predators can only take small mussels, predator recruitment may well depend upon the successful settlement of strong mussel cohorts. Evidence for such entrainment of predator cohorts to settlements of mussels is presented.     

Visual orientation by the crown-of-thorns starfish (<Emphasis Type="Italic">Acanthaster planci</Emphasis>)

Photoreception in echinoderms has been known for over 200 years, but their visual capabilities remain poorly understood. As has been reported for some asteroids, the crown-of-thorns starfish (Acanthaster planci) possess a seemingly advanced eye at the tip of each of its 7–23 arms. With such an array of eyes, the starfish can integrate a wide field of view of its surroundings. We hypothesise that, at close range, orientation and directional movements of the crown-of-thorns starfish are visually guided. In this study, the eyes and vision of A. planci were examined by means of light microscopy, electron microscopy, underwater goniometry, electroretinograms and behavioural experiments in the animals’ natural habitat. We found that only animals with intact vision could orient to a nearby coral reef, whereas blinded animals, with olfaction intact, walked in random directions. The eye had peak sensitivity in the blue part (470 nm) of the visual spectrum and a narrow, horizontal visual field of approximately 100° wide and 30° high. With approximately 250 ommatidia in each adult compound eye and average interommatidial angles of 8°, crown-of-thorns starfish have the highest spatial resolution of any starfish studied to date. In addition, they have the slowest vision of all animals examined thus far, with a flicker fusion frequency of only 0.6–0.7 Hz. This may be adaptive as fast vision is not required for the detection of stationary objects such as reefs. In short, the eyes seem optimised for detecting large, dark, stationary objects contrasted against an ocean blue background. Our results show that the visual sense of the crown-of-thorns starfish is much more elaborate than has been thus far appreciated and is essential for orientation and localisation of suitable habitats.     

Decadal trends in a coral community and evidence of changed disturbance regime

A 23 year data set (1981–2003 inclusive) and the spatially explicit individual-based model “Compete^©” were used to investigate the implications of changing disturbance frequency on cover and taxonomic composition of a shallow coral community at Lizard Island, Australia. Near-vertical in situ stereo-photography was used to estimate rates of coral growth, mortality, recruitment and outcomes of pair-wise competitive interactions for 17 physiognomic groups of hard and soft corals. These data were used to parameterise the model, and to quantify impacts of three acute disturbance events that caused significant coral mortality: 1982—a combination of coral bleaching and Crown-of-Thorns starfish; 1990—cyclone waves; and 1996—Crown-of-Thorns starfish. Predicted coral community trajectories were not sensitive to the outcomes of competitive interactions (probably because average coral cover was only 32% and there was strong vertical separation among established corals) or to major changes in recruitment rates. The model trajectory of coral cover matched the observed trajectory accurately until the 1996 disturbance, but only if all coral mortality was confined to the 3 years of acute disturbance. Beyond that date (1997–2003), when the observed community failed to recover, it was necessary to introduce annual chronic background mortality to obtain a good match between modelled and observed coral cover. This qualitative switch in the model may reflect actual loss of resilience in the real community. Simulated over a century, an 8 year disturbance frequency most closely reproduced the mean community composition observed in the field prior to major disturbance events. Shorter intervals between disturbances led to reduced presence of the dominant hard coral groups, and a gradual increase in the slow growing, more resilient soft corals, while longer intervals (up to 16 years) resulted in monopolization by the fastest growing table coral, Acropora hyacinthus.     

Brown-band syndrome on feeding scars of the crown-of-thorn starfish Acanthaster?planci

Despite the growing impact of coral diseases on reef ecosystems, little is known about the role of coral predation in disease transmission. An experiment on the coral reefs of Derawan Island, Indonesia, revealed brown-band syndrome on Acropora cytherea coral colonies following predation by the crown-of-thorn starfish Acanthaster planci. To experimentally exclude predation, living coral tissue adjacent to feeding scars was enclosed using cages and monitored for 15 days. Compared with similarly caged but uninjured colonies, which showed no sign of disease or tissue loss, preyed upon colonies showed a higher incidence of the disease, coupled with further tissue mortality. This study provides preliminary evidence that A. planci might promote the transmission of some coral diseases.     

Coral reef environmental science: truth versus the Cassandra syndrome

In 1970, coral reef science was warned that the crown-of-thorns starfish, Acanthaster planci, might cause the extinction of scleractinian corals in the Pacific Ocean. Now, 20 years later we can fortunately say that this alarm was almost certainly too severe. Many reefs were devastated by the starfish, but none are extinct, none have disappeared and many are in various stages of recovery. But now in the 1990's a new alarm is being sounded. This time the concern is over widespread destruction of coral reefs by elevated surface temperatures. Once again a few scientists have issued a dire warning that these events may represent a harbinger of ocean warming caused by the Greenhouse Effect. Has not Acanthaster taught coral reef science a lesson? The debate is far from over but this time the mood in general is not one of over-reaction. This time the Cassandras will be tested by the truth of careful experimentation, long-term monitoring and objective interpretation. Coral reef science appears to have come of age.     

Effects of coral bleaching on the feeding response of two species of coral-feeding fish

Coral bleaching is an increasingly prominent threat to coral reef ecosystems, not only to corals, but also to the many organisms that rely on coral for food and shelter. Coral-feeding fishes are negatively affected by coral loss caused by extensive bleaching, but it is unknown how feeding behaviour of most corallivorous fishes changes in response to coral bleaching. In this study, coral bleaching was experimentally induced in situ to examine the feeding response of two obligate corallivorous fish, Labrichthys unilineatus (Labridae) and Chaetodon baronessa (Chaetodontidae). Feeding rates were monitored before, during, and immediately after experimental bleaching of prey corals. L. unilineatus significantly increased its feeding on impacted corals during bleaching, but showed a steady decline in feeding once corals were fully bleached. Feeding response of L. unilineatus appears to parallel the expected stress-induced mucous production by bleaching colonies. In contrast, C. baronessa preferentially fed from healthy colonies over bleached colonies, although bleached colonies were consumed for five days following manipulation. Feeding by corallivorous fishes can play an important role in determining coral condition and mortality of corals following stress induced bleaching.     

A preliminary study of the biology and ecology of the blue starfish Linckia laevigata (L.) on the Australian Great Barrier Reef and an interpretation of its role in the coral reef ecosystem

The blue starfish Linckia laevigata grazes coralline algae. The starfish populations studied were composed entirely of adults. Spawning takes place in October at the southern end of the Great Barrier Reef. On reefs which were unaffected by Acanthaster planci, L. laevigata was confined to algae covered reef tops and rubble banks. On reefs affected by A. planci, L. laevigata had extended its range and was feeding on and among the coralline algae covered dead hard coral skeletons on the reef perimeter. Coral regrowth, followingattack by A. planci , was found to be slower on reefs with populations of L. laevigata living on the reef perimeter than on reefs where they were absent from this region. It is suggested that grazing by L. laevigata destroys small coral colonies and newly settled larvae thus slowing down the rate of coral regeneration. The consequences of this reduced rate of recolonisation is also discussed.     

Near-future ocean acidification enhances the feeding rate and development of the herbivorous juveniles of the crown-of-thorns starfish, <Emphasis Type="Italic">Acanthaster planci</Emphasis>

Population outbreaks of the corallivorous crown-of-thorns starfish, Acanthaster planci, are a major contributor to the decline in coral reef across the Indo-Pacific. The success of A. planci and other reef species in a changing ocean will be influenced by juvenile performance because the naturally high mortality experienced at this sensitive life history stage maybe exacerbated by ocean warming and acidification. We investigated the effects of increased temperature and acidification on growth of newly metamorphosed juvenile A. planci and their feeding rates on crustose coralline algae (CCA) during the initial herbivorous phase of their life history. The juveniles were exposed to three temperature (26, 28, 30 °C) and three pH (NIST scale: 8.1, 7.8, 7.6) levels in a flow-through cross-factorial experiment. There were positive but independent effects of warming and acidification on juvenile growth and feeding. Early juveniles were highly tolerant to moderate increases in temperature (+2 °C above ambient) with the highest growth at 30 °C. Growth and feeding rates of A. planci on CCA were highest at pH 7.6. Thus, ocean warming and acidification may enhance the success of A. planci juveniles. In contrast to its coral prey, at this vulnerable developmental stage, A. planci appears to be highly resilient to future ocean change. Success of juveniles in a future ocean may have carry-over effects into the coral-eating life stage, increasing the threat to coral reef systems.     

A gonad-stimulating peptide of the crown-of-thorns starfish,Acanthaster planci

The crown-of thorns starfish, Acanthaster planci, has been blamed for coral mortality in a large number of coral reef systems in the Indo-Pacific region. Because population outbreaks of A. planci are closely related to reproduction, it is important to examine the mechanism of reproductive control in this starfish. Previously, a relaxin-like gonad-stimulating peptide (RGP) in starfish Asterina pectinifera has been identified as the gonadotropin responsible for final gamete maturation. On the basis of homology research on RGP cDNAs from several species, this study was carried out to identify gonadotropin in A. planci. The cDNA sequence of RGP was determined using a RACE product of mRNA from the radial nerves of A. planci. The coding DNA sequence consisted of 351 base pairs with an open reading frame encoding a peptide of 116 amino acids (aa), including a signal peptide (29 aa), B-chain (19 aa), C-peptide (44 aa), and A-chain (24 aa). The chemical structure of A. planci RGP was exactly the same as that of A. pectinifera RGP. Furthermore, synthetic RGP could induce gamete spawning and oocyte maturation in the ovarian fragments of A. planci. This strongly suggested that the RGP is a gonadotropin in A. planci.     

Aposematic coloration does not deter corallivory by fish on the coral <Emphasis Type="Italic">Montastraea cavernosa</Emphasis>

Predation on corals by visual predators is a significant source of partial or total mortality on coral reefs, and corals have evolved strategies, including chemical defenses, to deter predation. One mechanism that organisms use to communicate the presence of chemical defenses is aposematic coloration, or the display of bright coloration as a warning to visual predators such as fish. Corals exhibit multiple colors, and it has been hypothesized that one role for this variability in coloration is as an aposematic warning of adverse palatability. Here, we test green and orange color morphs of the Caribbean coral Montastraea cavernosa for the presence of chemical defenses and whether their differences in coloration elicited different feeding responses. While M. cavernosa is chemically defended, there is no difference in feeding deterrence between color morphs; thus, the different color morphs of this coral species do not appear to represent an example of aposematic coloration.