Starfish Larvae Research Articles

Variable food alters responses of larval crown-of-thorns starfish to ocean warming but not acidification

Phytoplankton abundance is decreasing and becoming more variable as the ocean climate changes. We examine how low, high, and variable phytoplankton food supply affected the survival, development, and growth of larval crown-of-thorns starfish, Acanthaster sp. exposed to combined warming (26, 30 °C) and acidification (pH 8.0, 7.6). Larvae fed a low food ration are smaller, and develop slower and with more abnormalities than larvae fed a high ration. Larvae fed a variable food supply (low, followed by high ration) overcome the negative effects of low food on development rate and occurrence of abnormalities, but are 16–17% smaller than larvae fed the high ration continuously. Acidification (pH 7.6) slows growth and development and increases abnormalities regardless of the food regime. Warming slows growth and development, but these effects are mitigated by high food availability. As tropical oceans warm, the success of crown-of-thorns starfish larvae may depend on the abundance of their phytoplankton prey.

Single cell analysis of starfish (Patiria pectinifera) larvae

single cell analysis of starfish (Patiria pectinifera) larvae

A Relaxin-Like Gonad-Stimulating Peptide Appears in the Early Development of the Starfish Patiria pectinifera.

Relaxin-like gonad-stimulating peptide (RGP) is a hormone with gonadotropin-like activity in starfish. This study revealed that spawning inducing activity was detected in an extract of brachiolaria larvae of Patiria pectinifera. Spawning inducing activity in the extract was due to P. pectinifera RGP (PpeRGP), not 1-methyladenine. The expression of PpeRGP mRNA was also found in brachiolaria. Immunohistochemical observation with specific antibodies for PpeRGP showed that PpeRGP was distributed in the peripheral adhesive papilla of the brachiolaria arms. In contrast, PpeRGP was not detected in the adult rudiment or ciliary band regions, which are present in the neural system. These findings strongly suggest that RGP exists in the larvae before metamorphosis. Because gonads are not developed in starfish larvae, it seems likely that RGP plays another role other than gonadotropic action in the early development of starfish.

Ultrasound-activated ciliary bands for microrobotic systems inspired by starfish

Cilia are short, hair-like appendages ubiquitous in various biological systems, which have evolved to manipulate and gather food in liquids at regimes where viscosity dominates inertia. Inspired by these natural systems, synthetic cilia have been developed and utilized in microfluidics and microrobotics to achieve functionalities such as propulsion, liquid pumping and mixing, and particle manipulation. Here, we demonstrate ultrasound-activated synthetic ciliary bands that mimic the natural arrangements of ciliary bands on the surface of starfish larva. Our system leverages nonlinear acoustics at microscales to drive bulk fluid motion via acoustically actuated small-amplitude oscillations of synthetic cilia. By arranging the planar ciliary bands angled towards (+) or away (−) from each other, we achieve bulk fluid motion akin to a flow source or sink. We further combine these flow characteristics with a physical principle to circumvent the scallop theorem and realize acoustic-based propulsion at microscales. Finally, inspired by the feeding mechanism of a starfish larva, we demonstrate an analogous microparticle trap by arranging + and − ciliary bands adjacent to each other.

Crown-of-thorns starfish larvae are vulnerable to predation even in the presence of alternative prey

Many predators reported to feed on crown-of-thorns starfish (CoTS, Acanthaster spp.) are generalist and opportunistic feeders. However, research into predation on CoTS tends to examine these predator–prey interactions in isolation, and it remains unknown whether many potential predators will prey on CoTS when other, potentially more palatable, food sources are available. Assessing predatory responses to changes in prey availability is critical for gauging the capacity of predators to regulate prey populations. Here, we explored prey preferences and tested for prey switching across nine species of planktivorous damselfish offered varying densities of Pacific CoTS (Acanthaster cf. solaris) larvae versus larvae of a common and co-occurring starfish, Linckia laevigata. Results show that planktivorous damselfishes will consume crown-of-thorns starfish larvae, even in the presence of alternative prey. Feeding responses varied among the nine planktivorous predators with five damselfishes (Acanthochromis polyacanthus, Amblyglyphidodon curacao, Dascyllus reticulatus, Pomacentrus amboinensis and Pomacentrus moluccensis) exhibiting increased consumption of Acanthaster larvae with increasing density, despite the presence of alternative prey. Moreover, Abudefduf sexfasciatus and P. amboinensis exhibited preference for larvae of A. cf. solaris over larvae of L. laevigata. Despite these predation patterns, prey switching between starfish larvae was not observed. These results add to a growing body of evidence which suggests that predators of the early life stages of A. cf. solaris could be important in regulating settlement and recruitment patterns of this starfish, especially at low, non-outbreak, densities.

The role of retinoic acid signaling in starfish metamorphosis

BackgroundAlthough retinoic acid (RA) signaling plays a crucial role in the body patterning of chordates, its function in non-chordate invertebrates, other than its mediation of environmental cues triggering metamorphosis in cnidarians, is largely unknown. We investigated the role of RA signaling in the metamorphosis of starfish (Echinodermata).ResultsWe found that exogenous RA treatment induced metamorphosis in starfish larvae. In contrast, inhibitors of RA synthesis and RA receptors suppressed metamorphosis triggered by attachment to a substrate. Gene expressions of the RA signaling component were detected in competent larvae.ConclusionsThis study provides insight into the ancestral function of RA signaling, which is conserved in the metamorphosis of cnidarians and starfish.

Dynamic vortex arrays created by starfish larvae

This paper is associated with a video winner of a 2016 APS/DFD Milton van Dyke Award for work presented at the DFD Gallery of Fluid Motion. The original video is available from the Gallery of Fluid Motion, https://doi.org/10.1103/APS.DFD.2016.GFM.V0055

Potential Enhanced Survivorship of Crown of Thorns Starfish Larvae due to Near-Annual Nutrient Enrichment during Secondary Outbreaks on the Central Mid-Shelf of the Great Barrier Reef, Australia

The Great Barrier Reef (GBR) is currently experiencing widespread crown of thorns starfish (CoTS) outbreaks, as part of the fourth wave of outbreaks since 1962. It is believed that these outbreaks have become more frequent on the GBR and elsewhere in the Indo-Pacific and are associated with anthropogenic causes. The two widely accepted potential causes are (1) anthropogenic nutrient enrichment leading to the increased biomass of phytoplankton, the food of the planktonic stage of larval CoTS; and (2) the overfishing of predators in the juvenile to adult stages of CoTS, for example, commercially fished species such as coral trout. In this study, we show that the evidence for the nutrient enrichment causation hypothesis is strongly based on a large number of recent studies in the GBR. We also hypothesise that secondary outbreaks in the region between Cairns and Townsville can also be enhanced by nutrient enriched conditions associated with the annual nutrient discharge from Wet Tropics rivers.

Larval Survivorship and Settlement of Crown-of-Thorns Starfish (Acanthaster cf. solaris) at Varying Algal Cell Densities

The dispersal potential of crown-of-thorns starfish (CoTS) larvae is important in understanding both the initiation and spread of population outbreaks, and is fundamentally dependent upon how long larvae can persist while still retaining the capacity to settle. This study quantified variation in larval survivorship and settlement rates for CoTS maintained at three different densities of a single-celled flagellate phytoplankton, Proteomonas sulcata (1 × 103, 1 × 104, and 1 × 105 cells/mL). Based on the larval starvation hypothesis, we expected that low to moderate levels of phytoplankton prey would significantly constrain both survival and settlement. CoTS larvae were successfully maintained for up to 50 days post-fertilization, but larval survival differed significantly between treatments. Survival was greatest at intermediate food levels (1 × 104 cells/mL), and lowest at high (1 × 105 cells/mL) food levels. Rates of settlement were also highest at intermediate food levels and peaked at 22 days post-fertilization. Peak settlement was delayed at low food levels, probably reflective of delayed development, but there was no evidence of accelerated development at high chlorophyll concentrations. CoTS larvae were recorded to settle 17–43 days post-fertilization, but under optimum conditions with intermediate algal cell densities, peak settlement occurred at 22 days post-fertilization. Natural fluctuations in nutrient concentrations and food availability may affect the number of CoTS that effectively settle, but seem unlikely to influence dispersal dynamics.

Modus vivendi

Striking visualization of the flows generated by starfish larvae in their fluid environment offers unique insight into how these organisms live. The beautiful vortices they create betray a dynamic mechanism for trading swimming off against feeding.

Vortex arrays and ciliary tangles underlie the feeding–swimming trade-off in starfish larvae

Many marine invertebrates have larval stages covered in linear arrays of beating cilia, which propel the animal while simultaneously entraining planktonic prey. These bands are strongly conserved across taxa spanning four major superphyla, and they are responsible for the unusual morphologies of many invertebrate larvae. However, few studies have investigated their underlying hydrodynamics. Here, we study the ciliary bands of starfish larvae, and discover a beautiful pattern of slowly-evolving vortices that surrounds the swimming animals. Closer inspection of the bands reveals unusual ciliary "tangles" analogous to topological defects that break up and re-form as the animal adjusts its swimming stroke. Quantitative experiments and modeling demonstrate that these vortices create a physical tradeoff between feeding and swimming in heterogenous environments, which manifests as distinct flow patterns or "eigen-strokes" representing each behavior---potentially implicating neuronal control of cilia. This quantitative interplay between larval form and hydrodynamic function may generalize to other invertebrates with ciliary bands, and illustrates the potential effects of active boundary conditions in other biological and synthetic systems.

Localization of Neuropeptide Gene Expression in Larvae of an Echinoderm, the Starfish Asterias rubens.

Neuropeptides are an ancient class of neuronal signaling molecules that regulate a variety of physiological and behavioral processes in animals. The life cycle of many animals includes a larval stage(s) that precedes metamorphic transition to a reproductively active adult stage but, with the exception of Drosophila melanogaster and other insects, research on neuropeptide signaling has hitherto largely focused on adult animals. However, recent advances in genome/transcriptome sequencing have facilitated investigation of neuropeptide expression/function in the larvae of protostomian (e.g., the annelid Platynereis dumerilii) and deuterostomian (e.g., the urochordate Ciona intestinalis) invertebrates. Accordingly, here we report the first multi-gene investigation of larval neuropeptide precursor expression in a species belonging to the phylum Echinodermata—the starfish Asterias rubens. Whole-mount mRNA in situ hybridization was used to visualize in bipinnaria and brachiolaria stage larvae the expression of eight neuropeptide precursors: L-type SALMFamide (S1), F-type SALMFamide (S2), vasopressin/oxytocin-type, NGFFYamide, thyrotropin-releasing hormone-type, gonadotropin-releasing hormone-type, calcitonin-type and corticotropin-releasing hormone-type. Expression of only three of the precursors (S1, S2, NGFFYamide) was observed in bipinnaria larvae but by the brachiolaria stage expression of all eight precursors was detected. An evolutionarily conserved feature of larval nervous systems is the apical organ and in starfish larvae this comprises the bilaterally symmetrical lateral ganglia, but only the S1 and S2 precursors were found to be expressed in these ganglia. A prominent feature of brachiolaria larvae is the attachment complex, comprising the brachia and adhesive disk, which mediates larval attachment to a substratum prior to metamorphosis. Interestingly, all of the neuropeptide precursors examined here are expressed in the attachment complex, with distinctive patterns of expression suggesting potential roles for neuropeptides in the attachment process. Lastly, expression of several neuropeptide precursors is associated with ciliary bands, suggesting potential roles for the neuropeptides derived from these precursors in control of larval locomotion and/or feeding. In conclusion, our findings provide novel perspectives on the evolution and development of neuropeptide signaling systems and neuroanatomical insights into neuropeptide function in echinoderm larvae.

Crown-of-Thorns Starfish Larvae Can Feed on Organic Matter Released from Corals

Previous studies have suggested that Crown-of-Thorns starfish (COTS) larvae may be able to survive in the absence of abundant phytoplankton resources suggesting that they may be able to utilize alternative food sources. Here, we tested the hypothesis that COTS larvae are able to feed on coral-derived organic matter using labeled stable isotope tracers (13C and 15N). Our results show that coral-derived organic matter (coral mucus and associated microorganisms) can be assimilated by COTS larvae and may be an important alternative or additional food resource for COTS larvae through periods of low phytoplankton biomass. This additional food resource could potentially facilitate COTS outbreaks by reducing resource limitation.

Predation on crown-of-thorns starfish larvae by damselfishes

Examining the functional response of predators can provide insight into the role of predation in structuring prey populations and ecological communities. This study explored feeding behaviour and functional responses of planktivorous damselfishes when offered captive reared larvae of crown-of-thorns starfish, Acanthaster sp., with the aim of determining whether these predators could ever play a role in moderating outbreaks of Acanthaster sp. We examined predatory behaviour of 11 species of planktivorous damselfish, testing: (1) the relationship between predator size and predation rate, both within and among fish species; (2) consumption rates on larvae of Acanthaster sp. versus larvae of a common, co-occurring coral reef asteroid Linckia laevigata; (3) maximal feeding rates upon both Acanthaster sp. and L. laevigata; and (4) functional responses of planktivorous fishes to increasing densities of Acanthaster sp. Consumption rates of crown-of-thorns larvae by damselfishes were independent of predator size; however, there was a significant negative relationship between predator size and consumption rate of L. laevigata, when pooling across all predatory species. Some damselfishes, including Acanthochromis polyacanthus and Amblyglyphidodon curacao, consumed larval Acanthaster sp. at a greater rate than for L. laevigata. Most predatory species (all except A. curacao and Pomacentrus amboinensis) exhibited a Type II functional response whereby the increasing feeding rate decelerated with increasing prey density. In addition to revealing that a wide range of planktivorous fishes can prey upon larvae of Acanthaster sp., these data suggest that planktivorous damselfishes may have the capacity to buffer against population fluctuations of Acanthaster sp. Importantly, predators with Type II functional responses often contribute to stability of prey populations, though planktivorous fishes may be swamped by an abnormally high influx of larvae, potentially contributing to the characteristic population fluctuations of Acanthaster sp.

Evolution of Myeloid Cells.

In 1882, Elie Metchnikoff identified myeloid-like cells from starfish larvae responding to the invasion by a foreign body (rose thorn). This marked the origins for the study of innate immunity, and an appreciation that cellular immunity was well established even in these "primitive" organisms. This chapter focuses on these myeloid cells as well as the newest members of this family, the dendritic cells, and explores their evolutionary origins. Our goal is to provide evolutionary context for the development of the multilayered immune system of mammals, where myeloid cells now serve as central effectors of innate immunity and regulators of adaptive immunity. Overall, we find that core contributions of myeloid cells to the regulation of inflammation are based on mechanisms that have been honed over hundreds of millions of years of evolution. Using phagocytosis as a platform, we show how fairly simple beginnings have offered a robust foundation onto which additional control features have been integrated, resulting in central regulatory nodes that now manage multifactorial aspects of homeostasis and immunity.

Two macrophage migration inhibitory factors regulate starfish larval immune cell chemotaxis

Immune cell recruitment is critical step in the inflammatory response and associated diseases. However, the underlying regulatory mechanisms are poorly understood in invertebrates. Mesenchyme cells of the starfish larvae, which allowed Metchnikoff to complete his landmark experiments, are important model for analysis of immune cell migration. The present study investigated the role of macrophage migration inhibitory factor (MIF)--an evolutionarily conserved cytokine that is functionally similar to chemokines--in the larvae of the starfish Patiria (Asterina) pectinifera, which were found to possess two orthologs, ApMIF1 and ApMIF2. ApMIF1 and ApMIF2 clustered with mammalian MIF and its homolog D-dopachrome tautomerase (DDT), respectively, in the phylogenetic analysis. In contrast to the functional similarity between mammalian MIF and DDT, ApMIF1 knockdown resulted in the excessive recruitment of mesenchyme cells in vivo, whereas ApMIF2 deficiency inhibited the recruitment of these cells to foreign bodies. Mesenchyme cells migrated along a gradient of recombinant ApMIF2 in vitro, whereas recombinant ApMIF1 completely blocked ApMIF2-induced directed migration. Moreover, the expression patterns of ApMIF1 and ApMIF2 messenger RNA in bacteria-challenged mesenchyme cells were consistent with in vivo observations of cell behaviors. These results indicate that ApMIF1 and ApMIF2 act as chemotactic inhibitory and stimulatory factors, respectively, and coordinately regulate mesenchyme cell recruitment during the immune response in starfish larvae. This is the first report describing opposing functions for MIF- and DDT-like molecules. Our findings provide novel insight into the mechanisms underlying immune regulation in invertebrates.

First report of field sampling and identification of crown-of-thorns starfish larvae

First report of field sampling and identification of crown-of-thorns starfish larvae

Crown-of-thorns starfish

Crown-of-thorns starfish

Defense system by mesenchyme cells in bipinnaria larvae of the starfish, Asterina pectinifera

Here we characterize starfish larval mesenchyme cells, in terms of not only their phagocytic behavior, but also their structural and functional properties as a defense system. Our study reveals the following: (1) most mesenchyme cells construct a dynamic network structure beneath the body wall; (2) mesenchyme cells phagocytically respond to almost all foreign materials and form syncytial aggregates to conceal relatively large amounts and large sizes of foreign material; (3) the morphologies of the syncytial aggregates differ from one another depending on the species and the surface configuration of the cellular foreign material; (4) no mesenchyme cells respond to live mesenchyme cells even though they phagocytose chemically fixed cells; (5) mesenchyme cells phagocytose both cellular constituents effluxed from the ectodermal cells and foreign materials taken into the blastocoel through the body wall. Together, these results suggest that mesenchyme cells are equipped with a spectrum of abilities to engage in a defense system in starfish larva.

Developmental gene regulatory network architecture across 500 million years of echinoderm evolution.

Evolutionary change in morphological features must depend on architectural reorganization of developmental gene regulatory networks (GRNs), just as true conservation of morphological features must imply retention of ancestral developmental GRN features. Key elements of the provisional GRN for embryonic endomesoderm development in the sea urchin are here compared with those operating in embryos of a distantly related echinoderm, a starfish. These animals diverged from their common ancestor 520-480 million years ago. Their endomesodermal fate maps are similar, except that sea urchins generate a skeletogenic cell lineage that produces a prominent skeleton lacking entirely in starfish larvae. A relevant set of regulatory genes was isolated from the starfish Asterina miniata, their expression patterns determined, and effects on the other genes of perturbing the expression of each were demonstrated. A three-gene feedback loop that is a fundamental feature of the sea urchin GRN for endoderm specification is found in almost identical form in the starfish: a detailed element of GRN architecture has been retained since the Cambrian Period in both echinoderm lineages. The significance of this retention is highlighted by the observation of numerous specific differences in the GRN connections as well. A regulatory gene used to drive skeletogenesis in the sea urchin is used entirely differently in the starfish, where it responds to endomesodermal inputs that do not affect it in the sea urchin embryo. Evolutionary changes in the GRNs since divergence are limited sharply to certain cis-regulatory elements, whereas others have persisted unaltered.