Multiple stressor effects of near-future elevated seawater temperature and decreased pH on righting and escape behaviors of two common Antarctic gastropods

Warming seawater temperatures and ocean acidification on the coastal western Antarctic Peninsula pose unique challenges to stenothermal marine invertebrates. The present study examines prospective sub-lethal effects of elevated temperature, pCO2, and resultant decrease in seawater pH, on righting behavior and maximal escape speeds for two common gastropods, the limpet Nacella concinna (Strebel) and mesogastropod snail Margarella antarctica (Lamy). Replicate individuals held in individual containers were exposed to four combinations of seawater temperature (1.5 °C-current average, 3.5 °C-projected average by 2100) and pH (pH 8.0-current average, pH 7.8-projected average by 2100 as a result of elevated pCO2 levels) for a period of 6 weeks. Following this chronic exposure, righting behavior, determined for the limpets as proportion to right over 24 h and for snails as time to right, as well as maximum escape speed following contact with a sea star predator were measured. We found no significant differences in proportions of limpets displaying the capacity to right among the four temperature-pH treatments. However, there was a significant temperature-pH interaction effect for mean righting times in snails, indicating that the effect of pH on the time to right is dependent on temperature. We found no significant effects of temperature or pH on mean maximal escape speed in limpets. Additionally, we observed a significant temperature-pH interaction effect for mean maximal escape speed in snails. These interactive effects make it difficult to make clear predictions about how these environmental factors may impact behavioral responses.

Seawater carbonate chemistry, survival, metamorphosis and respiration rate of coral Acropora digitifera during experiments, 2011

Ocean acidification may negatively impact the early life stages of some marine invertebrates including corals. Although reduced growth of juvenile corals in acidified seawater has been reported, coral larvae have been reported to demonstrate some level of tolerance to reduced pH. We hypothesize that the observed tolerance of coral larvae to low pH may be partly explained by reduced metabolic rates in acidified seawater because both calcifying and non-calcifying marine invertebrates could show metabolic depression under reduced pH in order to enhance their survival. In this study, after 3-d and 7-d exposure to three different pH levels (8.0, 7.6, and 7.3), we found that the oxygen consumption of Acropora digitifera larvae tended to be suppressed with reduced pH, although a statistically significant difference was not observed between pH conditions. Larval metamorphosis was also observed, confirming that successful recruitment is impaired when metamorphosis is disrupted, despite larval survival. Results also showed that the metamorphosis rate significantly decreased under acidified seawater conditions after both short (2 h) and long (7 d) term exposure. These results imply that acidified seawater impacts larval physiology, suggesting that suppressed metabolism and metamorphosis may alter the dispersal potential of larvae and subsequently reduce the resilience of coral communities in the near future as the ocean pH decreases.

Molecular fingerprinting and amplicon sequencing of the bacterial biofilm on settlement tiles deployed along natural pH gradients in Papua New Guinea

Bacterial biofilms provide cues for the settlement of marine invertebrates such as coral larvae, and are therefore important for the resilience and recovery of coral reefs. This study aimed to better understand how ocean acidification may affect the community composition and diversity of bacterial biofilms on surfaces under naturally reduced pH conditions. Settlement tiles were deployed at coral reefs in Papua New Guinea along pH gradients created by two CO2 seeps, and upper and lower tiles surfaces were sampled 5 and 13 months after deployment. Automated Ribosomal Intergenic Spacer Analysis were used to characterize more than 200 separate bacterial communities, complemented by amplicon sequencing of the bacterial 16S rRNA gene of 16 samples. The bacterial biofilm consisted predominantly of Alpha-, Gamma- and Deltaproteobacteria, as well as Cyanobacteria, Flavobacteriia and Cytophaga, whereas putative settlement-inducing taxa only accounted for a small fraction of the community. Bacterial biofilm composition was heterogeneous with approximately 25% shared operational taxonomic units between samples. Among the observed environmental parameters, pH only had a weak effect on community composition (R² ~ 1%) and did not affect community richness and evenness. In contrast, there were strong differences between upper and lower surfaces (contrasting in light exposure and grazing intensity). There also appeared to be a strong interaction between bacterial biofilm composition and the macroscopic components of the tile community. Our results suggest that on mature settlement surfaces in situ, pH does not have a strong impact on the composition of bacterial biofilms. Other abiotic and biotic factors such as light exposure and interactions with other organisms may be more important in shaping bacterial biofilms than changes in seawater pH.

Giant clams and rising CO2: light may ameliorate effects of ocean acidification on a solar-powered animal

Global climate change and ocean acidification pose a serious threat to marine life. Marine invertebrates are particularly susceptible to ocean acidification, especially highly calcareous taxa such as molluscs, echinoderms and corals. The largest of all bivalve molluscs, giant clams, are already threatened by a variety of local pressures, including overharvesting, and are in decline worldwide. Several giant clam species are listed as 'Vulnerable' on the IUCN Red List of Threatened Species and now climate change and ocean acidification pose an additional threat to their conservation. Unlike most other molluscs, giant clams are 'solar-powered' animals containing photosynthetic algal symbionts suggesting that light could influence the effects of ocean acidification on these vulnerable animals. In this study, juvenile fluted giant clams Tridacna squamosa were exposed to three levels of carbon dioxide (CO2) (control ~400, mid ~650 and high ~950 µatm) and light (photosynthetically active radiation 35, 65 and 304 µmol photons/m**2/s). Elevated CO2 projected for the end of this century (~650 and ~950 µatm) reduced giant clam survival and growth at mid-light levels. However, effects of CO2 on survival were absent at high-light, with 100% survival across all CO2 levels. Effects of CO2 on growth of surviving clams were lessened, but not removed, at high-light levels. Shell growth and total animal mass gain were still reduced at high-CO2. This study demonstrates the potential for light to alleviate effects of ocean acidification on survival and growth in a threatened calcareous marine invertebrate. Managing water quality (e.g. turbidity and sedimentation) in coastal areas to maintain water clarity may help ameliorate some negative effects of ocean acidification on giant clams and potentially other solar-powered calcifiers, such as hard corals.

Does Encapsulation Protect Embryos from the Effects of Ocean Acidification? The Example of Crepidula fornicata

Early life history stages of marine organisms are generally thought to be more sensitive to environmental stress than adults. Although most marine invertebrates are broadcast spawners, some species are brooders and/or protect their embryos in egg or capsules. Brooding and encapsulation strategies are typically assumed to confer greater safety and protection to embryos, although little is known about the physico-chemical conditions within egg capsules. In the context of ocean acidification, the protective role of encapsulation remains to be investigated. To address this issue, we conducted experiments on the gastropod Crepidula fornicata. This species broods its embryos within capsules located under the female and veliger larvae are released directly into the water column. C. fornicata adults were reared at the current level of CO2 partial pressure (pCO2) (390 µatm) and at elevated levels (750 and 1400 µatm) before and after fertilization and until larval release, such that larval development occurred entirely at a given pCO2. The pCO2 effects on shell morphology, the frequency of abnormalities and mineralization level were investigated on released larvae. Shell length decreased by 6% and shell surface area by 11% at elevated pCO2 (1400 µatm). The percentage of abnormalities was 1.5- to 4-fold higher at 750 µatm and 1400 µatm pCO2, respectively, than at 390 µatm. The intensity of birefringence, used as a proxy for the mineralization level of the larval shell, also decreased with increasing pCO2. These negative results are likely explained by increased intracapsular acidosis due to elevated pCO2 in extracapsular seawater. The encapsulation of C. fornicata embryos did not protect them against the deleterious effects of a predicted pCO2 increase. Nevertheless, C. fornicata larvae seemed less affected than other mollusk species. Further studies are needed to identify the critical points of the life cycle in this species in light of future ocean acidification.

Juvenile sea stars exposed to acidification decrease feeding and growth with no acclimation potential

Ocean acidification has the potential to affect growth and calcification of benthic marine invertebrates, particularly during their early life history. We exposed field-collected juveniles of Asterias rubens from Kiel Fjord (western Baltic Sea) to 3 seawater CO2 partial pressure (pCO2) levels (ranging from around 650 to 3500 µatm) in a long-term (39 wk) and a short-term (6 wk) experiment. In both experiments, survival and calcification were not affected by elevated pCO2. However, feeding rates decreased strongly with increasing pCO2, while aerobic metabolism and NH4+ excretion were not significantly affected by CO2 exposure. Consequently, high pCO2 reduced the scope for growth in A. rubens. Growth rates decreased substantially with increasing pCO2 and were reduced even at pCO2 levels occurring in the habitat today (e.g. during upwelling events). Sea stars were not able to acclimate to higher pCO2, and growth performance did not recover during the long-term experiment. Therefore, the top-down control exerted by this keystone species may be diminished during periods of high environmental pCO2 that already occur occasionally and will be even higher in the future. However, some individuals were able to grow at high rates even at high pCO2, indicating potential for rapid adaption. The selection of adapted specimens of A. rubens in this seasonally acidified habitat may lead to higher CO2 tolerance in adult sea stars of this population compared to the juvenile stage. Future studies need to address the synergistic effects of multiple stressors such as acidification, warming and reduced salinity, which will simultaneously impact the performance of sea stars in this habitat.

Tough as a rock-boring urchin: adult Echinometra sp. EE from the Red Sea show high resistance to ocean acidification over long-term exposures

Ocean acidification, a process caused by the continuous rise of atmospheric CO2 levels, is expected to have a profound impact on marine invertebrates. Findings of the numerous studies conducted in this field indicate high variability in species responses to future ocean conditions. This study aimed at understanding the effects of long-term exposure to elevated pCO2 conditions on the performance of adult Echinometra sp. EE from the Gulf of Aqaba (Red Sea). During an 11-month incubation under high pCO2 (1,433 µatm, pHNBS 7.7) and control (435 µatm, pHNBS 8.1) conditions, we examined the urchins' somatic and gonadal growth, gametogenesis and skeletal microstructure. Somatic and gonadal growths were exhibited with no significant differences between the treatments. In addition, all urchins in the experiment completed a full reproductive cycle, typical of natural populations, with no detectable impact of increased pCO2 on the timing, duration or progression of the cycle. Furthermore, scanning electron microscopy imaging of urchin tests and spines revealed no signs of the usual observed effects of acidosis, such as skeletal dissolution, widened stereom pores or non-smoothed structures. Our results, which yielded no significant impact of the high pCO2 treatment on any of the examined processes in the urchins studied, suggest high resistance of adult Echinometra sp. EE to near future ocean acidification conditions. With respect to other findings in this area, the outcome of this study provides an example of the complicated and diverse responses of echinoids to the predicted environmental changes.

High-precision 40Ar/39Ar geochronology and the advent of North America’s Late Cretaceous terrestrial fauna

A densely sampled, diverse new fauna from the uppermost Cedar Mountain Formation, Utah, indicates that the basic pattern of faunal composition for the Late Cretaceous of North America was already established by the Albian-Cenomanian boundary. Multiple, concordant 40Ar/39Ar determinations from a volcanic ash associated with the fauna have an average age of 98.39 ± 0.07 million years. The fauna of the Cedar Mountain Formation records the first global appearance of hadrosaurid dinosaurs, advanced lizard (e.g., Helodermatidae), and mammal (e.g., Marsupialia) groups, and the first North American appearance of other taxa such as tyrannosaurids, pachycephalosaurs, and snakes. Although the origin of many groups is unclear, combined biostratigraphic and phylogenetic evidence suggests an Old World, specifically Asian, origin for some of the taxa, an hypothesis that is consistent with existing evidence from tectonics and marine invertebrates. Large-bodied herbivores are mainly represented by low-level browsers, ornithopod dinosaurs, whose radiations have been hypothesized to be related to the initial diversification of angiosperm plants. Diversity at the largest body sizes (>106 g) is low, in contrast to both preceding and succeeding faunas; sauropods, which underwent demise in the Northern hemisphere coincident with the radiation of angiosperms, apparently went temporarily unreplaced by other megaherbivores. Morphologic and taxonomic diversity among small, omnivorous mammals, multituberculates, is also low. A later apparent increase in diversity occurred during the Campanian, coincident with the appearance of major fruit types among angiosperms, suggesting the possibility of adaptive response to new resources.

Calcium release from the endoplasmic reticulum of higher plants elicited by the NADP metabolite nicotinic acid adenine dinucleotide phosphate

Higher plants share with animals a responsiveness to the Ca2+ mobilizing agents inositol 1,4,5-trisphosphate (InsP3) and cyclic ADP-ribose (cADPR). In this study, by using a vesicular 45Ca2+ flux assay, we demonstrate that microsomal vesicles from red beet and cauliflower also respond to nicotinic acid adenine dinucleotide phosphate (NAADP), a Ca2+-releasing molecule recently described in marine invertebrates. NAADP potently mobilizes Ca2+ with a K1/2 = 96 nM from microsomes of nonvacuolar origin in red beet. Analysis of sucrose gradient-separated cauliflower microsomes revealed that the NAADP-sensitive Ca2+ pool was derived from the endoplasmic reticulum. This exclusively nonvacuolar location of the NAADP-sensitive Ca2+ pathway distinguishes it from the InsP3- and cADPR-gated pathways. Desensitization experiments revealed that homogenates derived from cauliflower tissue contained low levels of NAADP (125 pmol/mg) and were competent in NAADP synthesis when provided with the substrates NADP and nicotinic acid. NAADP-induced Ca2+ release is insensitive to heparin and 8-NH2-cADPR, specific inhibitors of the InsP3- and cADPR-controlled mechanisms, respectively. However, NAADP-induced Ca2+ release could be blocked by pretreatment with a subthreshold dose of NAADP, as previously observed in sea urchin eggs. Furthermore, the NAADP-gated Ca2+ release pathway is independent of cytosolic free Ca2+ and therefore incapable of operating Ca2+-induced Ca2+ release. In contrast to the sea urchin system, the NAADP-gated Ca2+ release pathway in plants is not blocked by L-type channel antagonists. The existence of multiple Ca2+ mobilization pathways and Ca2+ release sites might contribute to the generation of stimulus-specific Ca2+ signals in plant cells.

Extraordinary divergence and positive Darwinian selection in a fusagenic protein coating the acrosomal process of abalone spermatozoa.

During fertilization in marine invertebrates, fusion between sperm and egg cell membranes occurs at the tip of the sperm acrosomal process. In abalone sperm the acrosomal process is coated with an 18-kDa protein. In situ, this protein has no effect on the egg vitelline envelope, but in vitro it is a potent fusagen of liposomes. Thus, the 18-kDa protein may mediate membrane fusion between the gametes, a step in gamete recognition known to restrict heterospecific fertilization in other species. The cDNA and deduced amino acid sequences of the 18-kDa protein were determined for five species of California abalone. The deduced amino acid sequences exhibit extraordinary divergence; the percent identity varies from 27% to 87%. Analysis of nucleotide substitution shows extremely high frequencies of amino acid-altering substitution compared to silent substitution, demonstrating that positive Darwinian selection promotes the divergence of this protein. However, amino acid replacement is conservative with respect to size and polarity of residue. The data support the developing idea that in free-spawning marine invertebrates, the proteins mediating fertilization may be subjected to intense, and as yet unknown, selective forces. The extraordinary divergence of fertilization proteins may be related to the establishment of barriers to heterospecific fertilization.

Sampling macroinvertebrates on high-energy sand beaches /

Includes glossary.

Die Zoophyten und Echinodermen des Adriatischen Meeres /

Mode of access: Internet.

Genetic variation of the scleractinian coral Stylophora pistillata, from western Pacific reefs

Most scleractinian coral species are widely distributed across the tropical and subtropical Indo-Pacific. However, the genetic connectivity between populations of corals separated by large distances (thousands of kilometers) is not well known. We analyzed variability in the nucleotide sequence of the internal transcribed spacer-1 (ITS-1) of the nuclear ribosomal gene unit in the ubiquitous coral Stylophora pistillata, across the western Pacific Ocean. Eight populations from Japan, Malaysia, and the northern and southern Great Barrier Reef (GBR) were studied. Phylogenetic analyses and analysis of molecular variance (AMOVA) clearly revealed that there is panmixia among these coral populations. AMOVA showed that ITS-1 sequence variability was greater within populations (78.37%) than among populations (12.06%). These patterns strongly suggest high levels of connectivity across the species' latitudinal distribution range in the western Pacific, as is seen in many marine invertebrates.

Coral reefs in a century of rapid environmental change

Coral reefs are the most diverse marine ecosystem and embrace possibly millions of plant, animal and protist species. Mutualistic symbioses are a fundamental feature of coral reefs that have been used to explain their structure, biodiversity and existence. Complex inter-relationships between hosts, habitats and symbionts belie closely coupled nutrient and community dynamics that create the circumstances for something from nothing (or the oasis in a nutrient desert). The flip side of these dynamics is a close dependency between species, which results in a series of non-linear relationships as conditions change. These responses are being highlighted as anthropogenic influences increase across the world's tropical and subtropical coastlines. Caribbean as well as Indo-Pacific coral populations are now in a serious decline in many parts of the world. This has resulted in a significant reorganization of how coral reef ecosystems function. Among the spectra of changes brought about by humans is rapid climate change. Mass coral bleaching - the loss of the dinoflagellate symbionts from reef-building corals - and mortality has affected the world's coral reefs with increasing frequency and intensity since the late 1970s. Mass bleaching events, which often cover thousands of square kilometres of coral reefs, are triggered by small increases (+1-3degreesC) in water temperature. These increases in sea temperature are often seen during warm phase weather conditions (e.g. ENSO) and are increasing in size and magnitude. The loss of living coral cover (e.g. 16% globally in 1998, an exceptionally warm year) is resulting in an as yet unspecified reduction in the abundance of a myriad of other species. Projections from general circulation models (GCM) used to project changes in global temperature indicate that conditions even under the mildest greenhouse gas emission scenarios may exceed the thermal tolerances of most reef-building coral communities. Research must now explore key issues such as the extent to which the thermal tolerances of corals and their symbionts are dynamic if bleaching and disease are linked; how the loss of high densities of reef-building coral will affect other dependent species; and, how the loss of coral populations will affect the millions of people globally who depend on coral reefs for their daily survival.

The effect of temperature on the size and population density of dinoflagellates in larvae of the reef coral Porites astreoides

Pre-settlement events play an important role in determining larval success in marine invertebrates with bentho-pelagic life histories, yet the consequences of these events typically are not well understood. The purpose of this study was to examine the pre-settlement impacts of different seawater temperatures on the size and population density of dinoflagellate symbionts in brooded larvae of the Caribbean coral Porites astreoides. Larvae were collected from P. astreoides at 14-20 m depth on Conch Reef (Florida) in June 2002, and incubated for 24 h at 15 temperatures spanning the range 25.1 degrees-30.0 degrees C in mean increments of 0.4 +/- 0.1 degrees C (+/- SD). The most striking feature of the larval responses was the magnitude of change in both parameters across this 5 degrees C temperature range within 24 h. In general, larvae were largest and had the highest population densities of Symbiodinium sp. between 26.4 degrees-27.7 degrees C, and were smallest and had the lowest population densities at 25.8 degrees C and 28.8 degrees C. Larval size and symbiont population density were elevated slightly (relative to the minimal values) at the temperature extremes of 25.1 degrees C and 30 degrees C. These data demonstrate that coral larvae are highly sensitive to seawater temperature during their pelagic phase, and respond through changes in size and the population densities of Symbiodinium sp. to ecologically relevant temperature signals within 24 h. The extent to which these changes are biologically meaningful will depend on the duration and frequency of exposure of coral larvae to spatio-temporal variability in seawater temperature, and whether the responses have cascading effects on larval success and their entry to the post-settlement and recruitment phase.