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.     

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.

     

Eye morphology and visual acuity in the pipevine swallowtail (Battus philenor) studied with a new method of measuring interommatidial angles

Because of the important role sensory systems play in the behaviour of animals, information on sensory capabilities is of great value to behavioural ecologists in the development of hypotheses to explain behaviour. In compound eyes, interommatidial angles are a key determinant of visual acuity but methods for measuring these angles are often demanding and limited to live animals with a pseudopupil. Here we present a new technique for measuring interommatidial angles that is less demanding in terms of technology than other techniques but still accurate. It allows measurements in eyes without a pseudopupil such as dark eyes or even museum specimens. We call this technique the radius of curvature estimation (RCE) method. We describe RCE and validate the method by comparing results from RCE with those from pseudopupil analysis for the butterfly Asterocampa leilia. As an application of RCE we measure the eyes of the butterfly Battus philenor, a species whose visually guided behaviour is well known but whose eye structure and visual acuity are unknown. We discuss the results of the eye morphology in B. philenor in relation to their behaviour and ecology. We contend that RCE fills a gap in the repertoire of techniques available to study peripheral determinants of spatial resolution in compound eyes, because it can be applied on species with dark eyes. RCE then opens up for sampling a larger number of specimens, which, in combination with being able to use museum specimens, makes it possible to quantitatively test ecologically and evolutionarily driven hypotheses about vision in animals in a new way.     

Sexual dimorphism in the visual system of flies: The divided brain of male Bibionidae (Diptera)

Summary The mapping of the compound eyes onto the visual neuropils and the cell types in the lamina and the lobula complex of Bibionidae (Diptera) were studied by means of extracellular cobalt injections and Golgi impregnations. Dorsal and ventral eyes in males map into separate dorsal-and ventral neuropils up to the level of the lobula complex. The dorsal-eye lamina is unilayered, while the ventral-eye lamina in males and the lamina in females are multilayered: layers A and C are invaded by en-passant terminals of long visual fibres, layer B by the terminals of short visual fibres. Long visual fibres have a short and a long terminal in the ventral medulla with terminal specialisations in three distinct layers. Only one type of receptor ending exists in the dorsal medulla, the terminal branches of which are restricted to one layer only. Arrays of contralateral neurones are found in the medial part of the dorsal lobula, which receives input from the zone of binocular vision of the ipsilateral dorsal eye, and in the posterior dorsal lobula and lobula plate. The dorsal lobula plate contains large tangential neurones, the dendritic arborisations of which are revealed by cobalt injection into the thoracic ganglia. The divided brain of male bibionids offers the opportunity to investigate separately the nervous systems involved in sex-specific visually guided flight behaviour and in general visually guided flight control.     

Visual signals in the courtship of Drosophila melanogaster: Mutant analysis

Visual cues are necessary for optimal mating success in Drosophila melanogaster. The male's most important visually guided behaviour is tracking. It is shown here that tracking requires intact visual receptor cells R1–6 and the presence of screening pigments in the eye. Thus flies carrying the mutation ebony as well as wild type flies affected in receptor cell R1–6 are unable to use visual cues when they track females. A similar defect was obseved in white-eyed flies lacking screening pigments. Female receptivity depends on visual signals provided by the male flies. Most important cues are the light reflection from and the shape of the male's eyes. No influence of the light reflected from the thorax could be seen. Absence of eyes in the male, however, does not depress female receptivity as much as white eyes. Some evidence is provided that male courtship behaviour is evaluated visually by the female.     

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.     

Geological evidence for recurring outbreaks of the crown-of-thorns starfish: a reassessment from an ecological perspective

The abundance and distribution of Acanthaster planci skeletal elements in reef sediments have been presented as evidence that population outbreaks of the crown-of-thorns starfish on the Great Barrier Reef are not a new occurrence, but have been an integral part of the ecosystem for at least 7000 years on some reefs (Walbran et al. 1989a). Reassessment of the evidence shows that these claims are not justified and challenges the validity of several assumptions that are crucial to their thesis that outbreaks have been a recurrent phenomenon on the Great Barrier Reef. These are: (i) that the majority of starfish from outbreak populations remain and die on the host reef and that their skeletal elements add to the reef sediment, (ii) that reefs which have had recent A. planci outbreaks can be discriminated from those which have not by the abundance of starfish skeletal remains in recent sediments, (iii) that outbreaks will significantly increase the number of skeletal elements in reef sediments above normal background levels and, (iv) that the age of individual skeletal elements can be predicted from the age of their surrounding sediment or their depth in the sediment pile. We conclude that Walbran et al. do not have sufficient data to infer the outbreak history of A. planci from the sediment recored and that there are alternative interpretations of their findings. The possibility cannot be discounted that destructive population outbreaks of A. planci witnessed on the Great Barrier Reef since 1960 are unprecedented. The question of whether A. planci outbreaks are a naturally recurring phenomena or a novel, more recent development remains unanswered.     

Highly hydroxylated steroids of the starfish Archaster typicus from the Vietnamese waters

Five new steroidal compounds, including an unusual glucoside, along with several known steroids were isolated from the starfish Archaster typicus collected in shallow waters of Quang Ninh province (Vietnam). Three new compounds are 27-nor-cholestane derivatives and the other two are 24,26-dihydroxycholestane derivatives. A biogenesis pathway for the unusual side chain of 27-nor-cholestane derivatives is proposed. Isolated compounds presented moderate toxic effects in the sperm- and 8-blastomere tests on embryonal development of the sea urchin Strongylocentrotusintermedius.     

The lens eyes of the box jellyfish <Emphasis Type="Italic">Tripedalia cystophora</Emphasis> and <Emphasis Type="Italic">Chiropsalmus sp.</Emphasis> are slow and color-blind

Box jellyfish, or cubomedusae, possess an impressive total of 24 eyes of four morphologically different types. Compared to other cnidarians they also have an elaborate behavioral repertoire, which for a large part seems to be visually guided. Two of the four types of cubomedusean eyes, called the upper and the lower lens eye, are camera type eyes with spherical fish-like lenses. Here we explore the electroretinograms of the lens eyes of the Caribbean species, Tripedalia cystophora, and the Australian species, Chiropsalmus sp. using suction electrodes. We show that the photoreceptors of the lens eyes of both species have dynamic ranges of about 3 log units and slow responses. The spectral sensitivity curves for all eyes peak in the blue-green region, but the lower lens eye of T. cystophora has a small additional peak in the near UV range. All spectral sensitivity curves agree well with the theoretical absorbance curve of a single opsin, strongly suggesting color-blind vision in box jellyfish with a single receptor type. A single opsin is supported by selective adaptation experiments.     

Scene perception and the visual control of travel direction in navigating wood ants

This review reflects a few of Mike Land''s many and varied contributions to visual science. In it, we show for wood ants, as Mike has done for a variety of animals, including readers of this piece, what can be learnt from a detailed analysis of an animal''s visually guided eye, head or body movements. In the case of wood ants, close examination of their body movements, as they follow visually guided routes, is starting to reveal how they perceive and respond to their visual world and negotiate a path within it. We describe first some of the mechanisms that underlie the visual control of their paths, emphasizing that vision is not the ant''s only sense. In the second part, we discuss how remembered local shape-dependent and global shape-independent features of a visual scene may interact in guiding the ant''s path.     

Differential scaling within an insect compound eye

Environmental and genetic influences cause individuals of a species to differ in size. As they do so, organ size and shape are scaled to available resources whilst maintaining function. The scaling of entire organs has been investigated extensively but scaling within organs remains poorly understood. By making use of the structure of the insect compound eye, we show that different regions of an organ can respond differentially to changes in body size. Wood ant (Formica rufa) compound eyes contain facets of different diameters in different regions. When the animal body size changes, lens diameters from different regions can increase or decrease in size either at the same rate (a ‘grade’ shift) or at different rates (a ‘slope’ shift). These options are not mutually exclusive, and we demonstrate that both types of scaling apply to different regions of the same eye. This demonstrates that different regions within a single organ can use different rules to govern their scaling, responding differently to their developmental environment. Thus, the control of scaling is more nuanced than previously appreciated, diverse responses occurring even among homologous cells within a single organ. Such fine control provides a rich substrate for the diversification of organ morphology.     

Taphonomy of crown-of-thorns starfish: implications for recognizing ancient population outbreaks

A field experiment was conducted to determine whether in situ mass mortality of Acanthaster planci subsequent to a simulated outbreak would leave a recognizable signature in surficial reef sediments. Constituent particle analyses comparing sediments that received starfish carcasses to those that did not revealed that, after a four year interval, the mass mortality was reflected by elevated abundances of starfish ossicles in 1–2 mm and 2–4 mm size classes, but not in >4 mm and 0.5–1 mm size classes. Additional field study of starfish taphonomy revealed that the abundance of starfish ossicles in surficial sediments decreases through two orders of magnitude between two weeks and four years post-mortem, while tumbling experiments suggest that the size distribution of starfish ossicles is modified by physical processes: the <0.5 mm size classes increases at the expense of the >4 mm class. Taphonomic biasing increased the abundance of crown-of-thorms starfish (COTS) skeletal elements in the 0.5–1 mm size fraction, while the 1–2 mm size and 2–4 mm fractions produced the most reliable signature of starfish mass mortality based on element abundance. Our results demonstrate the importance of taphonomic processes in altering the original size frequency distribution of the COTS skeleton and their potential for biasing predictions of past population levels derived from constituent particle analyses of surficial reef sediments.     

Steroidal monoglycosides from the Far Eastern starfish Hippasteria kurilensis and hypothetic pathways of polyhydroxysteroid biosynthesis in starfish

Five new steroidal monoglycosides, kurilensosides E (1), F (2), G (3), H (4) and 15-O-sulfate of echinasteroside C (5) were isolated along with the previously known echinasteroside C (6) from the alcoholic extract of the Far Eastern starfish Hippasteria kurilensis collected near Kuril Islands. Compounds 1-3 were determined to contain unusual polyhydroxysteroidal aglycons lacking 6-hydroxy group. Aglycon moiety of kurilensoside H (4) was shown to be the first case of marine polar steroids containing 4,5-epoxy functionality. Hypothetic pathways of the biosynthesis of polyhydroxysteroids and related glycosides in starfish and the existence of the late C-6 oxidation pathway in H. kurilensis are discussed.     

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.     

Aspects of the ecology of the coral-eating starfish Acanthaster planci

In the central region of the Great Barrier Reef, Acanthaster planci eats its own disk area of coral each day. At the southern end of the reef lagoon populations of A. planci eat substantially less than this amount of coral per day. Branching and plate corals are preferred food species and massive and encrusting forms are rejected while the preferred food species are available. Only when branching and plate forms on a reef have been consumed will A. planci attack massive and encrusting species. On Australian reefs preferred food species form between 70–99% of the coral cover.
On the Great Barrier Reef A. planci spawns in January and juveniles settle in the top 3 m of water on the windward edge of reefs or on isolated patch reefs behind the main reef. Intolerance of wave attack forces the growing starfish to migrate into deeper water. Lateral movements, probably induced by shortage of living coral in deep water, bring the starfish around the ends of the reef to the leeward side. Here they destroy most of the living coral.
It is suggested that the visual impact of A. planci on reefs of the Indo-Pacific region is related to the composition of the coral fauna. Reefs with a high proportion of preferred food species will be severely damaged while those with faunas composed mainly of massive and encrusting forms will not be altered greatly by starfish predation.
Work on larval development of A. planci carried out by Henderson & Lucas, 1971 showed that metamorphosis took place only at water temperatures of 28^o -29^o C. This suggests that the A. planci plague on the Great Barrier Reef will not spread south of latitude 20^o S (29^o C isotherm in January).     

Active sensing in a freely walking spider: look where to go

The Central American hunting spider Cupiennius salei, like most other spiders, has eight eyes, one pair of principal eyes and three pairs of secondary eyes. The principal eyes and one pair of the secondary eyes have almost completely overlapping visual fields, and presumably differ in function. The retinae of the principal eyes can be moved independently by two pairs of eye muscles each, whereas the secondary eyes do not have such eye muscles. The behavioural relevance of retinal movements of freely moving spiders was investigated by a novel dual-channel telemetric registration of the eye muscle activities. Walking spiders shifted the ipsilateral retina with respect to the walking direction before, during and after a turning movement. The change in the direction of vision in the ipsilateral anterior median eye was highly correlated with the walking direction, regardless of the actual light conditions. The contralateral retina remained in its resting position. This indicates that Cupiennius salei shifts it visual field in the walking direction not only during but sometimes previous to an intended turn, and therefore “peers” actively into the direction it wants to turn.     

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.     

A Simple Behavioral Assay for Testing Visual Function in Xenopus laevis

Measurement of the visual function in the tadpoles of the frog, Xenopus laevis, allows screening for blindness in live animals. The optokinetic response is a vision-based, reflexive behavior that has been observed in all vertebrates tested. Tadpole eyes are small so the tail flip response was used as alternative measure, which requires a trained technician to record the subtle response. We developed an alternative behavior assay based on the fact that tadpoles prefer to swim on the white side of a tank when placed in a tank with both black and white sides. The assay presented here is an inexpensive, simple alternative that creates a response that is easily measured. The setup consists of a tripod, webcam and nested testing tanks, readily available in most Xenopus laboratories. This article includes a movie showing the behavior of tadpoles, before and after severing the optic nerve. In order to test the function of one eye, we also include representative results of a tadpole in which each eye underwent retinal axotomy on consecutive days. Future studies could develop an automated version of this assay for testing the vision of many tadpoles at once.     

Male-specific (Z)-9-tricosene stimulates female mating behaviour in the spider Pholcus beijingensis

Chemical signals play an important role in spider sexual communication, yet the chemistry of spider sex pheromones remains poorly understood. Chemical identification of male-produced pheromone-mediating sexual behaviour in spiders has also, to our knowledge, not been reported before. This study aimed to examine whether chemically mediated strategies are used by males of the spider Pholcus beijingensis for increasing the probability of copulation. Based on data from gas chromatography–mass spectrometry analysis, electroantennography assay and a series of behavioural tests, we verified that (Z)-9-tricosene is a male-specific compound in the spider P. beijingensis. This compound acts as an aphrodisiac: it increases the likelihood that a female will mate. Mate-searching males release (Z)-9-tricosene to stimulate sexual behaviour of conspecific females. In the two-choice assay, however, sexually receptive females show no preference to the chambers containing (Z)-9-tricosene. This indicates that the male pheromone of P. beijingensis is not an attractant per se to the conspecific females. This is, to our knowledge, the first identification of a male-produced aphrodisiac pheromone in spiders.