Jane E. Williamson

Near-future levels of ocean acidification reduce fertilization success in a sea urchin

Summary Although it is widely believed that seawater is chemically well-buffered, CO 2 -induced acidification of the worlds oceans threatens the viability of many species [1–3]. Research to date has focused on the responses of adult stages of calcifying taxa to gross pH changes relevant for the years 2200–2400 [3,4]. We investigated the consequences of exposure of gametes and larvae of the sea urchin Heliocidaris erythrogramma to CO 2 -induced acidification by −0.4 pH units (the upper limit of predictions for the year 2100 [5]), and found statistically significant reductions in sperm swimming speed and percent sperm motility. We predicted the effects of these changes using an established model [6], and tested fertilization success experimentally in assays using the same gametes and pH treatments. Observed reductions in fertilization success corresponded closely to model predictions (24% reduction). If general, these findings have important implications for the reproductive and population viability of broadcast spawning marine species in the future acidified ocean.

Oceanic variability and coastal topography shape genetic structure in a long-dispersing sea urchin.

Understanding the scale of marine population connectivity is critical for the conservation and sustainable management of marine resources. For many marine species adults are benthic and relatively immobile, so patterns of larval dispersal and recruitment provide the key to understanding marine population connectivity. Contrary to previous expectations, recent studies have often detected unexpectedly low dispersal and fine-scale population structure in the sea, leading to a paradigm shift in how marine systems are viewed. Nonetheless, the link between fine-scale marine population structure and the underlying physical and biological processes has not been made. Here we show that patterns of genetic structure and population connectivity in the broadcast-spawning and long-distance dispersing sea urchin Centrostephanus rodgersii are influenced by physical oceanographic and geographic variables. Despite weak genetic differentiation and no isolation-by-distance over thousands of kilometers among samples from eastern Australia and northern New Zealand, fine-scale genetic structure was associated with sea surface temperature (SST) variability and geography along the southeastern Australian coast. The zone of high SST variability is characterized by periodic shedding of eddies from the East Australian Current, and we suggest that ocean current circulation may, through its influence on larval transport and recruitment, interact with the genetic consequences of large variance in individual reproductive success to generate patterns of fine-scale patchy genetic structure. If proven consistent across species, our findings suggest that the optimal scale for fisheries management and reserve design should vary among localities in relation to regional oceanographic variability and coastal geography.

Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae

Bacterial biofilms are increasingly seen as important for the successful settlement of marine invertebrate larvae. Here we tested the effects of biofilms on settlement of the sea urchin Heliocidaris erythrogramma. Larvae settled on many surfaces including various algal species, rocks, sand and shells. Settlement was reduced by autoclaving rocks and algae, and by treatment of algae with antibiotics. These results, and molecular and culture-based analyses, suggested that the bacterial community on plants was important for settlement. To test this, approximately 250 strains of bacteria were isolated from coralline algae, and larvae were exposed to single-strain biofilms. Many induced rates of settlement comparable to coralline algae. The genus Pseudoalteromonas dominated these highly inductive strains, with representatives from Vibrio, Shewanella, Photobacterium and Pseudomonas also responsible for a high settlement response. The settlement response to different bacteria was species specific, as low inducers were also dominated by species in the genera Pseudoalteromonas and Vibrio. We also, for the first time, assessed settlement of larvae in response to characterised, monospecific biofilms in the field. Larvae metamorphosed in higher numbers on an inducing biofilm, Pseudoalteromonas luteoviolacea, than on either a low-inducing biofilm, Pseudoalteromonas rubra, or an unfilmed control. We conclude that the bacterial community on the surface of coralline algae is important as a settlement cue for H. erythrogramma larvae. This study is also an example of the emerging integration of molecular microbiology and more traditional marine eukaryote ecology.

Induction of Settlement of Larvae of the Sea Urchin Holopneustes purpurascens by Histamine From a Host Alga

Larvae of the Australian sea urchin Holopneustes purpurascens are induced to settle and metamorphose (termed settlement herein) by a water-soluble compound produced by the red alga Delisea pulchra, the main host plant of new recruits. The settlement cue for H. purpurascens had previously been identified as a floridoside-isethionic acid complex, and this paper presents new evidence correcting that finding. The actual settlement cue produced by D. pulchra was isolated from the polar extract by cation-exchange chromatography and identified as histamine, using one- and two-dimensional nuclear magnetic resonance spectrometry. The chemical identity of the cue was confirmed by gas chromatography–mass spectrometry (GC-MS) and matrix-assisted laser desorption/ionization–time-of-flight mass spectrometry. Synthetic histamine and histamine at 4.5 μM isolated from D. pulchra both induced rapid settlement in 80%–100% of the larvae of H. purpurascens. Lower concentrations of histamine (0.9–2.3 μM) induced larval settlement, but this response varied from 0%–90%. The histamine content of two host plants of H. purpurascens—D. pulchra and Ecklonia radiata—and of four other common species was quantified using GC-MS. D. pulchra had the highest histamine content, which is consistent with H. purpurascens recruiting to this species. Histamine was also detected in the seawater surrounding these host algae. This is the first time that a settlement cue has been quantified in the habitat of a marine organism.

Individual Variability in Reproductive Success Determines Winners and Losers under Ocean Acidification: A Case Study with Sea Urchins

Background Climate change will lead to intense selection on many organisms, particularly during susceptible early life stages. To date, most studies on the likely biotic effects of climate change have focused on the mean responses of pooled groups of animals. Consequently, the extent to which inter-individual variation mediates different selection responses has not been tested. Investigating this variation is important, since some individuals may be preadapted to future climate scenarios. Methodology/Principal Findings We examined the effect of CO2-induced pH changes (“ocean acidification”) in sperm swimming behaviour on the fertilization success of the Australasian sea urchin Heliocidaris erythrogramma, focusing on the responses of separate individuals and pairs. Acidification significantly decreased the proportion of motile sperm but had no effect on sperm swimming speed. Subsequent fertilization experiments showed strong inter-individual variation in responses to ocean acidification, ranging from a 44% decrease to a 14% increase in fertilization success. This was partly explained by the significant relationship between decreases in percent sperm motility and fertilization success at ΔpH = 0.3, but not at ΔpH = 0.5. Conclusions and Significance The effects of ocean acidification on reproductive success varied markedly between individuals. Our results suggest that some individuals will exhibit enhanced fertilization success in acidified oceans, supporting the concept of ‘winners’ and ‘losers’ of climate change at an individual level. If these differences are heritable it is likely that ocean acidification will lead to selection against susceptible phenotypes as well as to rapid fixation of alleles that allow reproduction under more acidic conditions. This selection may ameliorate the biotic effects of climate change if taxa have sufficient extant genetic variation upon which selection can act.

Induction of metamorphosis in the sea urchin Holopneustes purpurascens by a metabolite complex from the algal host Delisea pulchra

Most benthic invertebrates have complex life cycles with planktonic larvae that return to the substratum to settle and metamorphose into a benthic stage. Although naturally produced chemical cues have long been thought to be important for the settlement or metamorphosis of invertebrate larvae, few ecologically relevant chemical cues have been clearly identified. The marine echinoid Holopneustes purpurascens has a complex life cycle, with a planktonic, nonfeeding dispersive larva that metamorphoses into a benthic stage that lives in the canopy of subtidal benthic algae such as the red alga Delisea pulchra and the kelp Ecklonia radiata. Recently recruited juveniles are found primarily on D. pulchra, and we hypothesized that this was in response to a chemical cue produced by this alga. Competent larvae metamorphosed in the presence of D. pulchra, or seawater surrounding this alga, but not in response to the presence of E. radiata or its extracts. A cue for metamorphosis was isolated and characterized from D. pulchra and found to be a water-soluble complex of the sugar floridoside and isethionic acid in a 1:1 molar ratio. The floridoside-isethionic acid complex also triggered settlement in H. purpurascens; however, this response was less specific than metamorphosis and was reversible. Larvae of H. purpurascens also metamorphosed in the presence of several other species of red, but not brown or green, algae from their habitat. Floridoside is found only in red algae, suggesting that the floridoside-isethionic acid complex may be acting as a cue for metamorphosis in other red algae as well as in D. pulchra.

Genetic structure of a recent climate change-driven range extension.

The life‐history strategies of some species make them strong candidates for rapid exploitation of novel habitat under new climate regimes. Some early‐responding species may be considered invasive, and negatively impact on ‘naïve’ ecosystems. The barrens‐forming sea urchin Centrostephanus rodgersii is one such species, having a high dispersal capability and a high‐latitude range margin limited only by a developmental temperature threshold. Within this species’ range in eastern Australian waters, sea temperatures have increased at greater than double the global average rate. The coinciding poleward range extension of C. rodgersii has caused major ecological changes, threatening reef biodiversity and fisheries productivity. We investigated microsatellite diversity and population structure associated with range expansion by this species. Generalized linear model analyses revealed no reduction in genetic diversity in the newly colonized region. A ‘seascape genetics’ analysis of genetic distances found no spatial genetic structure associated with the range extension. The distinctive genetic characteristic of the extension zone populations was reduced population‐specific FST, consistent with very rapid population expansion. Demographic and genetic simulations support our inference of high connectivity between pre‐ and post‐extension zones. Thus, the range shift appears to be a poleward extension of the highly‐connected rangewide population of C. rodgersii. This is consistent with advection of larvae by the intensified warm water East Australian current, which has also increased Tasmanian Sea temperatures above the species’ lower developmental threshold. Thus, ocean circulation changes have improved the climatic suitability of novel habitat for C. rodgersii and provided the supply of recruits necessary for colonization.

It pays to cheat : tactical deception in a cephalopod social signalling system

Signals in intraspecific communication should be inherently honest; otherwise the system is prone to collapse. Theory predicts, however, that honest signalling systems are susceptible to invasion by cheats, the extent of which is largely mediated by fear of reprisal. Cuttlefish facultatively change their shape and colour, an ability that evolved to avoid predators and capture prey. Here, we show that this ability is tactically employed by male mourning cuttlefish (Sepia plangon) to mislead conspecifics during courtship in a specific social context amenable to cheating 39 per cent of the time, while it was never employed in other social contexts. Males deceive rival males by displaying male courtship patterns to receptive females on one side of the body, and simultaneously displaying female patterns to a single rival male on the other, thus preventing the rival from disrupting courtship. The use of tactical deception in such a complex communication network indicates that sociality has played a key role in the cognitive evolution of cephalopods.

Collaborative photo-identification and monitoring of grey nurse sharks (Carcharias taurus) at key aggregation sites along the eastern coast of Australia

Before the worldwide decline of the ‘globally vulnerable’ Carcharias taurus may be addressed, an understanding of its migratory patterns and locations, and/or times when sharks may be vulnerable, is required to identify habitats that are critical to its survival. A collaborative framework for photo-identification and monitoring of C. taurus may greatly assist with conservation management initiatives. Images of C. taurus were sourced from public submissions to the www.spotashark.com (verified 12 February 2009) website and during targeted surveys. A computer-assisted program (I3S) was used to match the images of sharks photographically from the database. Research revealed patterns of movement, site utilisation and population structure similar to those in previous tagging studies. With the use of an underwater camera and two laser-scaling devices, 408 individual sharks were identified. Average occupancy times at two locations in New South Wales (NSW), Australia, were 308 days (Fish Rock) and 363 days (Magic Point). Seventeen individuals undertook northward or southward movements, averaging 350 km. The present study showed that a broad-based technique for data acquisition, coupled with rigorous evaluation of photographic identifications can provide support for local research and management programs and may aid with the conservation of the C. taurus species worldwide.

Dietary niche differentiation of five sympatric species of Platycephalidae

The dietary composition and partitioning of food resources between five sympatric species of Platycephalidae inhabiting the coastal waters of New South Wales, Australia was investigated. Samples were collected monthly between March and November 2007 onboard commercial ocean prawn trawlers based in the ports of Yamba and Newcastle. Monthly percentage weight contribution of 12 prey categories was analysed to determine if diet was influenced by the variables: species, location, depth, size and maturity. Of the 959 stomachs from the five species examined, 28–54% contained prey. All Platycephalid species primarily consumed teleosts, however the diversity of prey and the proportion each prey type contributed to the overall diet varied substantially between species. Platycephalus caeruleopunctatus, P. longispinis, P. richardsoni and Ambiserrula jugosa were generalist carnivores and consumed prey from a wide variety of phyla including teleosts, crustaceans, polychaetes, molluscs and echinoderms. In contrast, Ratabulus diversidens were primarily piscivorous. Partitioning of prey resources between species was more evident in waters at Yamba than at Newcastle. Differences in diet between locations were considered a result of differential prey exploitation rather than shifts in the suite of prey consumed. Dietary composition was observed to be influenced by size, maturity status and depth however these differences were not observed for all species.