Juvenile waiting stage crown-of-thorns sea stars are resilient in heatwave conditions that bleach and kill corals.

The juveniles of predatory sea stars can remain in their recruitment-nursery habitat for some time before their ontogenetic shift to the adult habitat and diet. These small juveniles are vulnerable to a range of factors with their sensitivity amplified by climate change-driven ocean warming. We investigate the thermal tolerance of the waiting stage herbivorous juveniles of the keystone coral predator, the crown-of-thorns sea star (COTS, Acanthaster sp.), in context with the degree heating weeks (DHW) model that predicts coral bleaching and mass mortality. In temperature treatments ranging from +1 to 3°C in prolonged heatwave acclimation conditions, the juveniles exhibited ~100% survival in DHW scenarios that trigger coral bleaching (4 DHW), resulting in mass mortality of corals (8 DHW) and extreme conditions well beyond those that kill corals (12 DHW). This indicates that herbivorous juvenile COTS are far more resistant to heatwave conditions than the coral prey of the adults. The juveniles exhibited higher activity (righting) and metabolic rate after weeks in increased temperature. In separate acute temperature experiments, the upper thermal limit of the juveniles was 34-36°C. In a warming world, juvenile COTS residing in their coral rubble nursery habitat will benefit from an increase in the extent of this habitat due to coral mortality. The juveniles have potential for long-term persistence as herbivores as they wait for live coral to recover before becoming coral predators, thereby serving as a proximate source of COTS outbreaks on reefs already in a tenuous state due to climate change.

Biochemical metabolomic profiling of the Crown-of-Thorns Starfish (Acanthaster): New insight into its biology for improved pest management.

The Crown-of-Thorns Starfish (COTS), Acanthaster species, is a voracious coral predator that destroys coral reefs when in outbreak status. The baseline metabolite and lipid biomolecules of 10 COTS tissues, including eggs from gravid females, were investigated in this study to provide insight into their biology and identify avenues for control. Targeted and untargeted metabolite- and lipidomics-based mass spectrometry approaches were used to obtain tissue-specific metabolite and lipid profiles. Across all COTS tissues, 410 metabolites and 367 lipids were identified. Most abundant were amino acids and peptides (18.7%) and wax esters (17%). There were 262 metabolites and 192 lipids identified in COTS eggs. Wax esters were more abundant in the eggs (30%) followed by triacylglycerols (TG), amino acids, and peptides. The diversity of asterosaponins in eggs (34) was higher than in tissues (2). Several asterosaponins known to modulate sperm acrosome reaction were putatively identified, including glycoside B, asterosaponin-4 (Co-Aris III), and regularoside B (asterosaponin A). The saponins saponin A, thornasteroside A, hillaside B, and non-saponins dictyol J and axinellamine B which have been shown to possess defensive properties, were found in abundance in gonads, skin, and radial nerve tissues. Inosine and 2-hexyldecanoic acid are the most abundant metabolites in tissues and eggs. As a secondary metabolite of purine degradation, inosine plays an important role in purine biosynthesis, while 2-hexyldecanoic acid is known to suppress side-chain crystallization during the synthesis of amphiphilic macromolecules (i.e., phospholipids). These significant spatial changes in metabolite, lipid, and asterosaponin profiles enabled unique insights into key biological tissue-specific processes that could be manipulated to better control COTS populations. Our findings highlight COTS as a novel source of molecules with therapeutic and cosmetic properties (ceramides, sphingolipids, carnosine, and inosine). These outcomes will be highly relevant for the development of strategies for COTS management including chemotaxis-based biocontrol and exploitation of COTS carcasses for the extraction of commercial molecules.

Crown of thorns starfish life-history traits contribute to outbreaks, a continuing concern for coral reefs.

Crown of thorns starfish (COTS, Acanthaster sp.) are notorious for their destructive consumption of coral that decimates tropical reefs, an attribute unique among tropical marine invertebrates. Their populations can rapidly increase from 0-1 COTS ha-1 to more than 10-1000 COTS ha-1 in short order causing a drastic change to benthic communities and reducing the functional and species diversity of coral reef ecosystems. Population outbreaks were first identified to be a significant threat to coral reefs in the 1960s. Since then, they have become one of the leading causes of coral loss along with coral bleaching. Decades of research and significant investment in Australia and elsewhere, particularly Japan, have been directed towards identifying, understanding, and managing the potential causes of outbreaks and designing population control methods. Despite this, the drivers of outbreaks remain elusive. What is becoming increasingly clear is that the success of COTS is tied to their inherent biological traits, especially in early life. Survival of larval and juvenile COTS is likely to be enhanced by their dietary flexibility and resilience to variable food conditions as well as their phenotypically plastic growth dynamics, all magnified by the extreme reproductive potential of COTS. These traits enable COTS to capitalise on anthropogenic disturbances to reef systems as well as endure less favourable conditions.

Microbiome reduction and endosymbiont gain from a switch in sea urchin life history.

Animal gastrointestinal tracts harbor a microbiome that is integral to host function, yet species from diverse phyla have evolved a reduced digestive system or lost it completely. Whether such changes are associated with alterations in the diversity and/or abundance of the microbiome remains an untested hypothesis in evolutionary symbiosis. Here, using the life history transition from planktotrophy (feeding) to lecithotrophy (nonfeeding) in the sea urchin Heliocidaris, we demonstrate that the lack of a functional gut corresponds with a reduction in microbial community diversity and abundance as well as the association with a diet-specific microbiome. We also determine that the lecithotroph vertically transmits a Rickettsiales that may complement host nutrition through amino acid biosynthesis and influence host reproduction. Our results indicate that the evolutionary loss of a functional gut correlates with a reduction in the microbiome and the association with an endosymbiont. Symbiotic transitions can therefore accompany life history transitions in the evolution of developmental strategies.

Echidnas of the Sea: The Defensive Behavior of Juvenile and Adult Crown-of-Thorns Sea Stars.

AbstractCrown-of-thorns sea stars are one of the most ecologically important tropical marine invertebrates, with boom-bust population dynamics that influence the community structure of coral reefs. Although predation is likely to influence the development of population outbreaks, little is known about the defensive behavior of crown-of-thorns sea stars. Righting behavior after being overturned, a key defensive response in echinoderms, was investigated for the newly settled herbivorous juvenile, the corallivorous juvenile, and adult stages of crown-of-thorns sea stars. The average righting time of the newly settled juveniles (0.3-1.0-mm diameter) was 2.74 minutes. For the coral-eating juveniles (15-55-mm diameter), the righting time (mean = 6.24 min) was faster in larger juveniles, and the mean righting time of the adults was 6.28 minutes. During righting and in response to being lifted off of the substrate, the juveniles and adults exhibited an arm curling response, during which their arms closed over their oral side, often forming a spine ball, a feature not known for other asteroids. The righting and curling responses of the corallivorous juveniles were influenced by the presence of a natural enemy, a coral guard crab, which caused the juveniles to spend more time with their arms curled. These behaviors indicate that crown-of-thorns sea stars use their spines to protect the soft tissue of their oral side. The highly defended morphology and behavioral adaptations of crown-of-thorns sea stars are likely to have evolved as antipredator mechanisms. This points to the potential importance of predators in regulating their populations, which may have decreased in recent times due to fishing, a factor that may contribute to outbreaks.

The Waiting Stage, Prolonged Residency in Nursery Habitats by Juveniles of the Predatory Sea Star Marthasterias glacialis.

AbstractGrowth and recruitment of the sea star Marthasterias glacialis was followed over six years in Lough Hyne, southwest Ireland. Juveniles from a 2-mm radius were found on algae at <1-2-m depth following what appeared to be gregarious larval settlement. Data from Lough Hyne and Mulroy Bay (northwest Ireland) indicated that algal habitat serves as a nursery area for juveniles of M. glacialis. Successive size frequency modes of the juveniles at Lough Hyne indicated slow growth over 6 years, to a mean radius of 20 mm. The absence of additional recruitment allowed monitoring of a discrete population. Recruits in the nursery habitat over the six years remained as waiting stage juveniles, a Peter Pan group with delayed maturity subsisting on a diet of epibionts. An initial sharp decline in numbers indicated post-settlement mortality, with subsequent decline likely due to migration to the adjacent shelly habitat, where subadult M. glacialis (30-70-mm radius) lives. In this habitat, M. glacialis preys on small bivalves and eventually joins the adult (maximum radius = 280 mm) population on open sediment, where it feeds on large bivalves. Size frequency distributions of the juveniles and adults showed growth over the six years, with the waiting stage sea stars slowly merging in size with the adult population. It appears that the supply of new individuals into the adult population may take place six or more years following settlement. Strong connectivity between life stage habitats and prolonged recruitment into the adult population may contribute to balanced exploitation of infaunal prey.

Knowledge Gaps in the Biology, Ecology, and Management of the Pacific Crown-of-Thorns Sea Star Acanthaster sp. on Australia's Great Barrier Reef.

AbstractCrown-of-thorns sea stars (Acanthaster sp.) are among the most studied coral reef organisms, owing to their propensity to undergo major population irruptions, which contribute to significant coral loss and reef degradation throughout the Indo-Pacific. However, there are still important knowledge gaps pertaining to the biology, ecology, and management of Acanthaster sp. Renewed efforts to advance understanding and management of Pacific crown-of-thorns sea stars (Acanthaster sp.) on Australia's Great Barrier Reef require explicit consideration of relevant and tractable knowledge gaps. Drawing on established horizon scanning methodologies, this study identified contemporary knowledge gaps by asking active and/or established crown-of-thorns sea star researchers to pose critical research questions that they believe should be addressed to improve the understanding and management of crown-of-thorns sea stars on the Great Barrier Reef. A total of 38 participants proposed 246 independent research questions, organized into 7 themes: feeding ecology, demography, distribution and abundance, predation, settlement, management, and environmental change. Questions were further assigned to 48 specific topics nested within the 7 themes. During this process, redundant questions were removed, which reduced the total number of distinct research questions to 172. Research questions posed were mostly related to themes of demography (46 questions) and management (48 questions). The dominant topics, meanwhile, were the incidence of population irruptions (16 questions), feeding ecology of larval sea stars (15 questions), effects of elevated water temperature on crown-of-thorns sea stars (13 questions), and predation on juveniles (12 questions). While the breadth of questions suggests that there is considerable research needed to improve understanding and management of crown-of-thorns sea stars on the Great Barrier Reef, the predominance of certain themes and topics suggests a major focus for new research while also providing a roadmap to guide future research efforts.

Ocean acidification induces distinct transcriptomic responses across life history stages of the sea urchin Heliocidaris erythrogramma.

Ocean acidification (OA) from seawater uptake of rising carbon dioxide emissions impairs development in marine invertebrates, particularly in calcifying species. Plasticity in gene expression is thought to mediate many of these physiological effects, but how these responses change across life history stages remains unclear. The abbreviated lecithotrophic development of the sea urchin Heliocidaris erythrogramma provides a valuable opportunity to analyse gene expression responses across a wide range of life history stages, including the benthic, post-metamorphic juvenile. We measured the transcriptional response to OA in H. erythrogramma at three stages of the life cycle (embryo, larva, and juvenile) in a controlled breeding design. The results reveal a broad range of strikingly stage-specific impacts of OA on transcription, including changes in the number and identity of affected genes; the magnitude, sign, and variance of their expression response; and the developmental trajectory of expression. The impact of OA on transcription was notably modest in relation to gene expression changes during unperturbed development and much smaller than genetic contributions from parentage. The latter result suggests that natural populations may provide an extensive genetic reservoir of resilience to OA. Taken together, these results highlight the complexity of the molecular response to OA, its substantial life history stage specificity, and the importance of contextualizing the transcriptional response to pH stress in light of normal development and standing genetic variation to better understand the capacity for marine invertebrates to adapt to OA.

Diet flexibility and growth of the early herbivorous juvenile crown-of-thorns sea star, implications for its boom-bust population dynamics.

The ecology of the early herbivorous juvenile stage of the crown-of-thorns sea star (COTS, Acanthaster spp.) is poorly understood, yet the success of this life stage is key to generating population outbreaks that devastate coral reefs. Crustose coralline algae (CCA) has been considered to be the main diet of herbivorous juveniles. In this study, we show that COTS can avail of a range of algal food. Juveniles were reared on CCA, Amphiroa sp., and biofilm, and survived for 10 months on all three diets. The juveniles fed CCA and Amphiroa sp. reached 15-16.5 mm diameter at ~ 6 months and maintained this size for the rest the experiment (an additional ~4 months). Juveniles fed biofilm grew more slowly and to a smaller maximum size (~3 mm diameter). However, when juveniles were switched from biofilm to CCA they resumed growth to a new asymptotic size (~13.5 mm, 13-20 months). In diet choice experiments, juveniles did not show a preference between Amphiroa sp. and CCA, but generally avoided biofilm. Our results show that juvenile COTS grew equally well on CCA and Amphiroa sp. and can subsist on biofilm for months. Some juveniles, mostly from the biofilm diet treatment, decreased in size for a time and this was followed by recovery. Flexibility in diet, growth, and prolonged maintenance of asymptotic size indicates capacity for growth plasticity in herbivorous juvenile COTS. There is potential for juvenile COTS to persist for longer than anticipated and increase in number as they wait for the opportunity to avail of coral prey. These findings complicate our ability to predict recruitment to the corallivorous stage and population outbreaks following larval settlement and the ability to understand the age structure of COTS populations.

The hidden army: corallivorous crown-of-thorns seastars can spend years as herbivorous juveniles.

Crown-of-thorns seastar (COTS) outbreaks are a major threat to coral reefs. Although the herbivorous juveniles and their switch to corallivory are key to seeding outbreaks, they remain a black box in our understanding of COTS. We investigated the impact of a delay in diet transition due to coral scarcity in cohorts reared on crustose coralline algae for 10 months and 6.5 years before being offered coral. Both cohorts achieved an asymptotic size (16-18 mm diameter) on algae and had similar exponential growth on coral. After 6.5 years of herbivory, COTS were competent coral predators. This trophic and growth plasticity results in a marked age-size disconnect adding unappreciated complexity to COTS boom-bust dynamics. The potential that herbivorous juveniles accumulate in the reef infrastructure to seed outbreaks when favourable conditions arise has implications for management of COTS populations.