Biochemical investigation of two responses involved in the feeding behaviour of Acanthaster planci (L). I. Assay methods and preliminary results

Material obtained by simple biochemical fractionation of aqueous extracts of coral has been tested for its ability to induce responses normally associated with feeding on live corals in the crown-of-thorns starfish, Acanthaster planci (L.) With the use of a new assay method, it has been shown that both dialysable and non-dialysable components of aqueous coral extract cause cessation of movement, settlement, and eversion of the stomach as if over a whole coral. A second response, apparently of avoidance, seen as a starfish approaches a coral prior to feeding, has also been examined; it is evoked by the dialysable fraction of coral extract.     

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.     

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.     

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.     

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.     

Visual navigation in starfish: first evidence for the use of vision and eyes in starfish

Most known starfish species possess a compound eye at the tip of each arm, which, except for the lack of true optics, resembles an arthropod compound eye. Although these compound eyes have been known for about two centuries, no visually guided behaviour has ever been directly associated with their presence. There are indications that they are involved in negative phototaxis but this may also be governed by extraocular photoreceptors. Here, we show that the eyes of the coral-reef-associated starfish Linckia laevigata are slow and colour blind. The eyes are capable of true image formation although with low spatial resolution. Further, our behavioural experiments reveal that only specimens with intact eyes can navigate back to their reef habitat when displaced, demonstrating that this is a visually guided behaviour. This is, to our knowledge, the first report of a function of starfish compound eyes. We also show that the spectral sensitivity optimizes the contrast between the reef and the open ocean. Our results provide an example of an eye supporting only low-resolution vision, which is believed to be an essential stage in eye evolution, preceding the high-resolution vision required for detecting prey, predators and conspecifics.     

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.

     

Corals and starfish devastation of the great barrier reef: Aggregation methods

Aggregation methods allow one to replace a large scale dynamical system (micro-system) by a reduced dynamical system (macro-system) governing a small number of global variables. This aggregation of variables can be performed when two time scales exist, a fast time scale and a slow time scale. Perturbation theory allows to obtain an approximated aggregated dynamical system which describes the behaviour of a few number of slow time varying variables which are constants of motion of the fast part of the micro-system. Aggregation methods are applied to the case of the devastation of the great barrier reef by the starfishes. We recall the Antonelli/Kazarinoff model which implies a stable limit cycle for the corals and starfish populations. This prey-predator model describes the interactions between two species of corals and the starfish. Then, we generalize the Antonelli/Kazarinoff model to the case of two spatial patches with a fast part describing the starfish migration on the patches and the human manipulation of the communities by divers and, a slow part describing the growth and the interactions between the populations. We obtain an aggregated model governing the total coral densities on the patches and the total starfish population. This model can exhibit stable limit cycle oscillations and a Hopf bifurcation. The critical value of the bifurcation parameter is expressed in terms of the proportions of coral species and starfish on the two patches. This implies for example that rather than random killing of starfish by the Australian military, it may be better to send teams of divers to outbreaking reefs when they first occur who will then manipulate the community structure to increase protection.     

Coral reef cascades and the indirect effects of predator removal by exploitation

Fisheries exploitation provides the opportunity to examine the ecosystem‐scale biodiversity consequences of predator removal. We document predatory reef fish densities, coral‐eating starfish densities and coral reef structure along a 13‐island gradient of subsistence exploitation in Fiji. Along the fishing intensity gradient, predator densities declined by 61% and starfish densities increased by three orders of magnitude. Reef‐building corals and coralline algae declined by 35% and were replaced by non‐reef building taxa (mainly filamentous algae), as a result of starfish predation. Starfish populations exhibited thresholds and Allee‐type dynamics: population growth was negative under light fishing intensities and high predator densities, and positive on islands with higher fishing intensities and low predator densities. These results suggest the depletion of functionally important consumer species by exploitation can indirectly influence coral reef ecosystem structure and function at the scale of islands.     

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.     

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.     

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.     

No-take reserves protect coral reefs from predatory starfish

The crown-of-thorns starfish, Acanthaster planci, is a predator of corals that is a major management issue on coral reefs [1]. It occurs throughout the Indo–Pacific and shows boom–bust population dynamics with low background densities and intermittent outbreaks. Three waves of population outbreaks have affected Australia's Great Barrier Reef (GBR) since the 1960s. The waves of outbreaks appear to start 15°S [2] and progress southward through the central GBR (Figure 1A), causing major losses of living coral on many reefs across a large area and dwarfing losses from other disturbances such as storms or coral bleaching over the same period [3]. Humans can potentially influence starfish population dynamics by exploiting predators, though evidence to date is circumstantial. Extensive surveys in the GBR Marine Park (GBRMP) show that protection from fishing affects the frequency of outbreaks: the relative frequency of outbreaks on reefs that were open to fishing was 3.75 times higher than that on no-take reefs in the mid-shelf region of the GBR, where most outbreaks occur, and seven times greater on open reefs if all reefs were included. Although exploited fishes are unlikely to prey on starfish directly, trophic cascades could favour invertebrates that prey on juvenile starfish.     

Mantle defensive response of marine pulmonate Trimusculusperuvianus

The marine pulmonate Trimusculusperuvianus (Sowerby, 1835) which is found in caves or narrow crevices along the Chilean coast was studied to determine a possible chemical defense against the intertidal key predator Heliasterhelianthus. T.peruvianus releases a white secretion through the extended mantle animal covers, to contact with the tube feet of starfish. This behaviour significantly decreases predation of gastropod and it has not been described previously for members of the Trimusculidae family.     

Development of microsatellite loci in the common reef starfish Linckia laevigata and Linckia multifora

We isolated seven polymorphic microsatellite loci from the coral reef starfish Linckia laevigata??a common coral reef sea star distributed widely in the Indo-Pacific. The number of alleles ranged from 4 to 13, with an average of 7.4. The ranges of observed and expected heterozygosities were 0.367/0.933 and 0.332/0.840 for L. laevigata and 0.182/0.818 and 0.329/0.697 for L. multifora, respectively. All of these markers can also be used in the sister species Linckia multifora. These microsatellite loci will be useful for population and conservation genetic studies in coral reef ecosystems.     

Spatial resilience of the Great Barrier Reef under cumulative disturbance impacts

In the face of increasing cumulative effects from human and natural disturbances, sustaining coral reefs will require a deeper understanding of the drivers of coral resilience in space and time. Here we develop a high‐resolution, spatially explicit model of coral dynamics on Australia's Great Barrier Reef (GBR). Our model accounts for biological, ecological and environmental processes, as well as spatial variation in water quality and the cumulative effects of coral diseases, bleaching, outbreaks of crown‐of‐thorns starfish (Acanthaster cf. solaris), and tropical cyclones. Our projections reconstruct coral cover trajectories between 1996 and 2017 over a total reef area of 14,780 km², predicting a mean annual coral loss of ?0.67%/year mostly due to the impact of cyclones, followed by starfish outbreaks and coral bleaching. Coral growth rate was the highest for outer shelf coral communities characterized by digitate and tabulate Acropora spp. and exposed to low seasonal variations in salinity and sea surface temperature, and the lowest for inner‐shelf communities exposed to reduced water quality. We show that coral resilience (defined as the net effect of resistance and recovery following disturbance) was negatively related to the frequency of river plume conditions, and to reef accessibility to a lesser extent. Surprisingly, reef resilience was substantially lower within no‐take marine protected areas, however this difference was mostly driven by the effect of water quality. Our model provides a new validated, spatially explicit platform for identifying the reefs that face the greatest risk of biodiversity loss, and those that have the highest chances to persist under increasing disturbance regimes.     

The chemical cue tetrabromopyrrole from a biofilm bacterium induces settlement of multiple Caribbean corals

Microbial biofilms induce larval settlement for some invertebrates, including corals; however, the chemical cues involved have rarely been identified. Here, we demonstrate the role of microbial biofilms in inducing larval settlement with the Caribbean coral Porites astreoides and report the first instance of a chemical cue isolated from a marine biofilm bacterium that induces complete settlement (attachment and metamorphosis) of Caribbean coral larvae. Larvae settled in response to natural biofilms, and the response was eliminated when biofilms were treated with antibiotics. A similar settlement response was elicited by monospecific biofilms of a single bacterial strain, Pseudoalteromonas sp. PS5, isolated from the surface biofilm of a crustose coralline alga. The activity of Pseudoalteromonas sp. PS5 was attributed to the production of a single compound, tetrabromopyrrole (TBP), which has been shown previously to induce metamorphosis without attachment in Pacific acroporid corals. In addition to inducing settlement of brooded larvae (P. astreoides), TBP also induced larval settlement for two broadcast-spawning species, Orbicella (formerly Montastraea) franksi and Acropora palmata, indicating that this compound may have widespread importance among Caribbean coral species.     

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.     

Distribution of recent outbreaks of the crown-of-thorns starfish (Acanthaster planci) along the Great Barrier Reef: 1985–1986

A large survey program was conducted during 1985/1986 to determine the extent of activity of the crown-of-thorns starfish, Acanthaster planci, and its broad effects on the coral communities of the Great Barrier Reef (GBR). The perimeters of 228 reefs (about 9% of reefs in the GBR system) were surveyed within 1 year using rapid survey, manta tow techniques. These reefs encompassed the broad latitudinal and longitudinal gradients within the GBR. Approximately 27% (62 reefs) of the reefs surveyed had recently experienced (18%), or were experiencing (9%), an outbreak of the crown-of-thorns starfish. These outbreaks were mainly confined to reefs in the central third of the GBR (between Lizard Island and Townsville) and had affected, to varying degrees, approximately 65% of the reefs surveyed within this region. A greater proportion of mid-shelf reefs had experienced outbreaks than outer-shelf reefs, although this difference was not statistically significant. Of the small number of inner-shelf reefs surveyed, none had been recently affected by an outbreak. Large active outbreaks of starfish were reported on many of the reefs located off Townsville while much smaller outbreaks were found on several reefs at the southern end of the GBR, in the Swain Reef complex. Almost 86% of reefs currently experiencing an outbreak had moderate to high coral mortality over at least a third of their perimeters. Only 10% of reefs with active outbreaks had high coral mortality over most of their windward and leeward margins. A similar proportion of reefs had low to moderate coral mortality over less than a third of their perimeters.     

Observations on the settlement of the brachiolaria larvae of Stichaster australis (Verill) and Coscinasterias calamaria (Gray) (Echinodermata: Asteroidea) in the laboratory and on the shore

The settling behaviour is described and substratum preferences of advances brachiolaria larvae of Stichaster australis (Verrill) and Coscinasterias calamaria (Gray) were determined with larvae reared in the laboratory and the results correlated with field observations of habitat preferences of juvenile starfish at Maori Bay on the west coast of Auckland, New Zealand.C. calamaria larvae settled on almost any hard substratum provided it was coated with a ‘primary’ film. Recently metamorphosed C. calamaria could not be found at Maori Bay and it is inferred that there is low recruitment from the plankton to the Maori Bay population.S. australis larvae would only settle, metamorphose, and feed on the encrusting coralline alga Mesophyllum insigne (Foslie) Adey. Nursery areas of offshore boulders covered with this alga are present at Maori Bay and these were found to support populations of juvenile starfish. M. insigne appears to provide a stable and abundant food source for juvenile S. australis.