Symon A. Dworjanyn

Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios

Global warming is causing ocean warming and acidification. The distribution of Heliocidaris erythrogramma coincides with the eastern Australia climate change hot spot, where disproportionate warming makes marine biota particularly vulnerable to climate change. In keeping with near-future climate change scenarios, we determined the interactive effects of warming and acidification on fertilization and development of this echinoid. Experimental treatments (20–26°C, pH 7.6–8.2) were tested in all combinations for the ‘business-as-usual’ scenario, with 20°C/pH 8.2 being ambient. Percentage of fertilization was high (>89%) across all treatments. There was no difference in percentage of normal development in any pH treatment. In elevated temperature conditions, +4°C reduced cleavage by 40 per cent and +6°C by a further 20 per cent. Normal gastrulation fell below 4 per cent at +6°C. At 26°C, development was impaired. As the first study of interactive effects of temperature and pH on sea urchin development, we confirm the thermotolerance and pH resilience of fertilization and embryogenesis within predicted climate change scenarios, with negative effects at upper limits of ocean warming. Our findings place single stressor studies in context and emphasize the need for experiments that address ocean warming and acidification concurrently. Although ocean acidification research has focused on impaired calcification, embryos may not reach the skeletogenic stage in a warm ocean.

Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla

Background As the oceans simultaneously warm, acidify and increase in P CO2, prospects for marine biota are of concern. Calcifying species may find it difficult to produce their skeleton because ocean acidification decreases calcium carbonate saturation and accompanying hypercapnia suppresses metabolism. However, this may be buffered by enhanced growth and metabolism due to warming. Methodology/Principal Findings We examined the interactive effects of near-future ocean warming and increased acidification/P CO2 on larval development in the tropical sea urchin Tripneustes gratilla. Larvae were reared in multifactorial experiments in flow-through conditions in all combinations of three temperature and three pH/P CO2 treatments. Experiments were placed in the setting of projected near future conditions for SE Australia, a global change hot spot. Increased acidity/P CO2 and decreased carbonate mineral saturation significantly reduced larval growth resulting in decreased skeletal length. Increased temperature (+3°C) stimulated growth, producing significantly bigger larvae across all pH/P CO2 treatments up to a thermal threshold (+6°C). Increased acidity (-0.3-0.5 pH units) and hypercapnia significantly reduced larval calcification. A +3°C warming diminished the negative effects of acidification and hypercapnia on larval growth. Conclusions and Significance This study of the effects of ocean warming and CO2 driven acidification on development and calcification of marine invertebrate larvae reared in experimental conditions from the outset of development (fertilization) shows the positive and negative effects of these stressors. In simultaneous exposure to stressors the dwarfing effects of acidification were dominant. Reduction in size of sea urchin larvae in a high P CO2 ocean would likely impair their performance with negative consequent effects for benthic adult populations.

Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean

The most fragile skeletons produced by benthic marine calcifiers are those that larvae and juveniles make to support their bodies. Ocean warming, acidification, decreased carbonate saturation and their interactive effects are likely to impair skeletogenesis. Failure to produce skeleton in a changing ocean has negative implications for a diversity of marine species. We examined the interactive effects of warming and acidification on an abalone (Haliotis coccoradiata) and a sea urchin (Heliocidaris erythrogramma) reared from fertilization in temperature and pH/pCO2 treatments in a climatically and regionally relevant setting. Exposure of ectodermal (abalone) and mesodermal (echinoid) calcifying systems to warming (+2°C to 4°C) and acidification (pH 7.6–7.8) resulted in unshelled larvae and abnormal juveniles. Haliotis development was most sensitive with no interaction between stressors. For Heliocidaris, the percentage of normal juveniles decreased in response to both stressors, although a +2°C warming diminished the negative effect of low pH. The number of spines produced decreased with increasing acidification/pCO2, and the interactive effect between stressors indicated that a +2°C warming reduced the negative effects of low pH. At +4°C, the developmental thermal tolerance was breached. Our results show that projected near-future climate change will have deleterious effects on development with differences in vulnerability in the two species.

Towards a better understanding of medicinal uses of the brown seaweed Sargassum in Traditional Chinese Medicine: a phytochemical and pharmacological review.

ETHNOPHARMACOLOGICAL RELEVANCE For nearly 2000 years Sargassum spp., a brown seaweed, has been used in Traditional Chinese Medicine (TCM) to treat a variety of diseases including thyroid disease (e.g. goitre). AIMS OF THE REVIEW To assess the scientific evidence for therapeutic claims made for Sargassum spp. in TCM and to identify future research needs. BACKGROUND AND METHODS A systematic search for the use of Sargassum in classical TCM books was conducted and linked to a search for modern phytochemical and pharmacological data on Sargassum spp. retrieved from PubMed, Web of Knowledge, SciFinder Scholar and CNKI (in Chinese). RESULTS AND DISCUSSION The therapeutic effects of Sargassum spp. are scientifically plausible and may be explained partially by key in vivo and in vitro pharmacological activities of Sargassum, such as anticancer, anti-inflammatory, antibacterial and antiviral activities. Although the mechanism of actions is still not clear, the pharmacological activities could be mainly attributed to the major biologically active metabolites, meroterpenoids, phlorotanins and fucoidans. The contribution of iodine in Sargassum for treating thyroid related diseases seem to have been over estimated. CONCLUSIONS The bioactive compounds in Sargassum spp. appear to play a role as immunomodulators and could be useful in the treatment of thyroid related diseases such as Hashimotos thyroiditis. Further research is required to determine both the preventative and therapeutic role of Sargassum spp. in thyroid health.

Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities

Marine invertebrate gametes are being spawned into an ocean simultaneously warming, acidifying and increasing in pCO(2). Decreased pH/increased pCO(2) narcotizes sperm indicating that acidification may impair fertilization, exacerbating problems of sperm limitation, with dire implications for marine life. In contrast, increased temperature may have a stimulatory effect, enhancing fertilization. We investigated effects of ocean change on sea urchin fertilization across a range of sperm densities. We address two predictions: (1) low pH/increased pCO(2) reduces fertilization at low sperm density and (2) increased temperature enhances fertilization, buffering negative effects of acidification and increased pCO(2). Neither prediction was supported. Fertilization was only affected by sperm density. Increased acidification and pCO(2) did not reduce fertilization even at low sperm density and increased temperature did not enhance fertilization. It is important to identify where vulnerabilities lie across life histories and our results indicate that sea urchin fertilization is robust to climate change stressors. However, developmental stages may be vulnerable to ocean change.

Adaptive Capacity of the Habitat Modifying Sea Urchin Centrostephanus rodgersii to Ocean Warming and Ocean Acidification: Performance of Early Embryos

Background Predicting effects of rapid climate change on populations depends on measuring the effects of climate stressors on performance, and potential for adaptation. Adaptation to stressful climatic conditions requires heritable genetic variance for stress tolerance present in populations. Methodology/Principal Findings We quantified genetic variation in tolerance of early development of the ecologically important sea urchin Centrostephanus rodgersii to near-future (2100) ocean conditions projected for the southeast Australian global change hot spot. Multiple dam-sire crosses were used to quantify the interactive effects of warming (+2–4°C) and acidification (−0.3−0.5 pH units) across twenty-seven family lines. Acidification, but not temperature, decreased the percentage of cleavage stage embryos. In contrast, temperature, but not acidification decreased the percentage of gastrulation. Cleavage success in response to both stressors was strongly affected by sire identity. Sire and dam identity significantly affected gastrulation and both interacted with temperature to determine developmental success. Positive genetic correlations for gastrulation indicated that genotypes that did well at lower pH also did well in higher temperatures. Conclusions/Significance Significant genotype (sire) by environment interactions for both stressors at gastrulation indicated the presence of heritable variation in thermal tolerance and the ability of embryos to respond to changing environments. The significant influence of dam may be due to maternal provisioning (maternal genotype or environment) and/or offspring genotype. It appears that early development in this ecologically important sea urchin is not constrained in adapting to the multiple stressors of ocean warming and acidification. The presence of tolerant genotypes indicates the potential to adapt to concurrent warming and acidification, contributing to the resilience of C. rodgersii in a changing ocean.

Ingestion of microplastic has limited impact on a marine larva

There is increasing concern about the impacts of microplastics (<1 mm) on marine biota. Microplastics may be mistaken for food items and ingested by a wide variety of organisms. While the effects of ingesting microplastic have been explored for some adult organisms, there is poor understanding of the effects of microplastic ingestion on marine larvae. Here, we investigated the ingestion of polyethylene microspheres by larvae of the sea urchin, Tripneustes gratilla. Ingestion rates scaled with the concentration of microspheres. Ingestion rates were, however, reduced by biological fouling of microplastic and in the presence of phytoplankton food. T. gratilla larvae were able to egest microspheres from their stomach within hours of ingestion. A microsphere concentration far exceeding those recorded in the marine environment had a small nondose dependent effect on larval growth, but there was no significant effect on survival. In contrast, environmentally realistic concentrations appeared to have little effect. Overall, these results suggest that current levels of microplastic pollution in the oceans only pose a limited threat to T. gratilla and other marine invertebrate larvae, but further research is required on a broad range of species, trophic levels, and polymer types.

The stunting effect of a high CO2 ocean on calcification and development in sea urchin larvae, a synthesis from the tropics to the poles

The stunting effect of ocean acidification on development of calcifying invertebrate larvae has emerged as a significant effect of global change. We assessed the arm growth response of sea urchin echinoplutei, here used as a proxy of larval calcification, to increased seawater acidity/pCO2 and decreased carbonate mineral saturation in a global synthesis of data from 15 species. Phylogenetic relatedness did not influence the observed patterns. Regardless of habitat or latitude, ocean acidification impedes larval growth with a negative relationship between arm length and increased acidity/pCO2 and decreased carbonate mineral saturation. In multiple linear regression models incorporating these highly correlated parameters, pCO2 exerted the greatest influence on decreased arm growth in the global dataset and also in the data subsets for polar and subtidal species. Thus, reduced growth appears largely driven by organism hypercapnia. For tropical species, decreased carbonate mineral saturation was most important. No single parameter played a dominant role in arm size reduction in the temperate species. For intertidal species, the models were equivocal. Levels of acidification causing a significant (approx. 10–20+%) reduction in arm growth varied between species. In 13 species, reduction in length of arms and supporting skeletal rods was evident in larvae reared in near-future (pCO2 800+ µatm) conditions, whereas greater acidification (pCO2 1000+ µatm) reduced growth in all species. Although multi-stressor studies are few, when temperature is added to the stressor mix, near-future warming can reduce the negative effect of acidification on larval growth. Broadly speaking, responses of larvae from across world regions showed similar trends despite disparate phylogeny, environments and ecology. Larval success may be the bottleneck for species success with flow-on effects for sea urchin populations and marine ecosystems.

Direct and indirect effects of ocean acidification and warming on a marine plant–herbivore interaction

The impacts of climatic change on organisms depend on the interaction of multiple stressors and how these may affect the interactions among species. Consumer–prey relationships may be altered by changes to the abundance of either species, or by changes to the per capita interaction strength among species. To examine the effects of multiple stressors on a species interaction, we test the direct, interactive effects of ocean warming and lowered pH on an abundant marine herbivore (the amphipod Peramphithoe parmerong), and whether this herbivore is affected indirectly by these stressors altering the palatability of its algal food (Sargassum linearifolium). Both increased temperature and lowered pH independently reduced amphipod survival and growth, with the impacts of temperature outweighing those associated with reduced pH. Amphipods were further affected indirectly by changes to the palatability of their food source. The temperature and pH conditions in which algae were grown interacted to affect algal palatability, with acidified conditions only affecting feeding rates when algae were also grown at elevated temperatures. Feeding rates were largely unaffected by the conditions faced by the herbivore while feeding. These results indicate that, in addition to the direct effects on herbivore abundance, climatic stressors will affect the strength of plant–herbivore interactions by changes to the susceptibility of plant tissues to herbivory.

Impacts of Ocean Acidification on Early Life-History Stages and Settlement of the Coral-Eating Sea Star Acanthaster planci

Coral reefs are marine biodiversity hotspots, but their existence is threatened by global change and local pressures such as land-runoff and overfishing. Population explosions of coral-eating crown of thorns sea stars (COTS) are a major contributor to recent decline in coral cover on the Great Barrier Reef. Here, we investigate how projected near-future ocean acidification (OA) conditions can affect early life history stages of COTS, by investigating important milestones including sperm motility, fertilisation rates, and larval development and settlement. OA (increased pCO2 to 900–1200 µatm pCO2) significantly reduced sperm motility and, to a lesser extent, velocity, which strongly reduced fertilization rates at environmentally relevant sperm concentrations. Normal development of 10 d old larvae was significantly lower under elevated pCO2 but larval size was not significantly different between treatments. Settlement of COTS larvae was significantly reduced on crustose coralline algae (known settlement inducers of COTS) that had been exposed to OA conditions for 85 d prior to settlement assays. Effect size analyses illustrated that reduced settlement may be the largest bottleneck for overall juvenile production. Results indicate that reductions in fertilisation and settlement success alone would reduce COTS population replenishment by over 50%. However, it is unlikely that this effect is sufficient to provide respite for corals from other negative anthropogenic impacts and direct stress from OA and warming on corals.