Inhibition of settlement and metamorphosis of the ascidian Herdmania curvata by non-geniculate coralline algae

The surfaces of non-geniculate coralline algae (NCA) are known to induce the settlement and metamorphosis of disparate marine taxa. In this study we investigate the responsiveness of larvae of Herdmania curvata (Ascidiacea: Stolidobranchia) to three species of NCA (Neo-goniolithon brassica-florida, Hydrolithon onkodes, and Lithothamnium prolifer) that cohabit the slope and crest of Heron Reef, Great Barrier Reef. H. curvata larvae were first exposed to these NCA at or within 2 h of hatching, which is 1 to 2 h prior to attaining competence, and then cultured continuously with the NCA for 12 to 14 h. Rates of settlement and metamorphosis of H, curvata cultured in laboratory chambers in the presence of the different NCA were significantly lower than spontaneous rates in seawater. The limited settlement in treatments containing NCA were confined entirely to the chamber periphery, and settlement never occurred on the surface of the NCA. The inhibitory effect was dose-dependent and was stronger in H. brassica-florida and H. onkodes than in L. prolifer. Larvae that did not settle in treatments with NCA had rounded anterior trunks and, in extreme cases, kinked tails with rounded and dissociated tail muscle cells. In some individuals, we observed the anterior chemosensory papillae being sloughed off the larval body. Morphological analysis of trunk ectodermal and mesenchymal nuclei of larvae cultured in the presence of the NCA revealed that general necrotic cell death was occurring. Importantly, H. curvata larvae that were exposed to NCA could not subsequently be induced to metamorphose in KCl-elevated seawater, whereas larvae not exposed to NCA metamorphosed at high rates in KCl-elevated seawater.

Rhodolith forming coralline algae in the Upper Miocene of Santa Maria Island (Azores, NE Atlantic) : a critical evaluation

The Late Miocene Malbusca outcrop is located in the southeastern coast of Santa Maria Island (Azores, NE Atlantic), interspersed in volcanic formations. At ~20 meters above present sea level, a prominent discontinuous layer of rhodoliths seizes with an extension of ~250 meters. This paper presents the first taxonomic record of fossil rhodolith forming coralline algae for the Miocene of the Azores. The preserved taxonomic features used were the following: (1) arrangement of basal filaments, (2) epithallial cells (when observable), (3) presence of cell fusions, (4) conceptacle type, (5) number of cells layers which conceptacle chamber floors are situated below the surrounding thallus surface and (6) for the sporangial pores, the orientation of the filaments around the conceptacle pores. Based on these characters, six taxa were identified encompassing three Corallinaceae (Lithophyllum prototypum, Lithophyllum sp., Spongites sp., Hydrolithon sp.) and one Hapalidaceae (Phymatolithon calcareum and cf. Phymatolithon sp.). An unidentified coaxial thallus was also present, the coaxial construction ascribing the specimens to the genus Mesophyllum or Neogoniolithon. Taxonomic accounts for the identified taxa are described, illustrated and an identification key is provided. The report of L prototypum represents the first Miocene record and the preservation of the specimens is very good. Miocene coralline algae seem very consistent among deposits but some species are relevant for particular areas, like in the Azores.

Twentieth Century Delta δC Variability in Surface Water Dissolved Inorganic Carbon Recorded by Coralline Algae in the Northern North Pacific Ocean and the Bering Sea

The oxygen isotopic composition and Mg/Ca ratios in the skeletons of long-lived coralline algae record ambient seawater temperature over time. Similarly, the carbon isotopic composition in the skeletons record delta(13)C values of ambient seawater dissolved inorganic carbon. Here, we measured delta(13)C in the coralline alga Clathromorphum nereostratum to test the feasibility of reconstructing the intrusion of anthropogenic CO(2) into the northern North Pacific Ocean and Bering Sea. The delta(13)C was measured in the high Mgcalcite skeleton of three C. nereostratum specimens from two islands 500 km apart in the Aleutian archipelago. In the records spanning 1887 to 2003, the average decadal rate of decline in delta(13)C values increased from 0.03% yr(-1) in the 1960s to 0.095% yr(-1) in the 1990s, which was higher than expected due to solely the delta(13)C-Suess effect. Deeper water in this region exhibits higher concentrations of CO(2) and low delta(13)C values. Transport of deeper water into surface water (i.e., upwelling) increases when the Aleutian Low is intensified. We hypothesized that the acceleration of the delta(13)C decline may result from increased upwelling from the 1960s to 1990s, which in turn was driven by increased intensity of the Aleutian Low. Detrended delta(13)C records also varied on 4-7 year and bidecadal timescales supporting an atmospheric teleconnection of tropical climate patterns to the northern North Pacific Ocean and Bering Sea manifested as changes in upwelling.

Lithothamnion Prolifer Foslie: A Common Non-Geniculate Coralline Alga (Rhodophyta: Corallinaceae) from the Tropical and Subtropical Indo-Pacific

A little-known, but ecologically important non-geniculate coralline, Lithothamnion prolifer, is recorded from a number of tropical Indo-Pacific sites, including Fiji, Australia, Kiribati and Indonesia. The species occurs primarily on vertical walls of caves and overhangs in Fiji and Australia, but was also found as rhodoliths in Kiribati. Lithothamnion prolifer is characterized by the combination of characters which follow. The thallus is extremely glossy, smooth, and rosy coloured. Thalli usually produce complanate protuberances, but protuberances become terete when growing on well lit, horizontal substrata, when unattached, or when growing on loose substrata. Conceptacles occur mainly on the tips of protuberances, and tetra/bisporangial conceptacles are large (to 1300 mu m external diameter, with chambers up to 1100 mu m diameter). The tetra/bisporangial conceptacles are flush or only slightly raised, and often extensive and irregularly shaped (resembling small sori). They lack a raised rim, and have flattened pore plates. The rosette cells surrounding the tetra/bisporangial pore appear somewhat sunken below the surrounding roof cells in SEM, and the cells of filaments lining the pore canals of tetra/bisporangial conceptacles do not differ from the cells of filaments making up the rest of the roof. Old conceptacles persist and become buried in the thallus, and are then usually completely filled in by irregularly arranged calcified cells.

Dolomite-rich coralline algae in reefs resist dissolution in acidified conditions

Coral reef ecosystems develop best in high-flow environments but their fragile frameworks are also vulnerable to high wave energy. Wave-resistant algal rims, predominantly made up of the crustose coralline algae (CCA) Porolithon onkodes and P. pachydermum, are therefore critical structural elements for the survival of many shallow coral reefs. Concerns are growing about the susceptibility of CCA to ocean acidification because CCA Mg-calcite skeletons are more susceptible to dissolution under low pH conditions than coral aragonite skeletons. However, the recent discovery of dolomite (Mg0.5Ca0.5(CO3)), a stable carbonate, in P. onkodes cells necessitates a reappraisal of the impacts of ocean acidification on these CCA. Here we show, using a dissolution experiment, that dried dolomite-rich CCA have 6-10 times lower rates of dissolution than predominantly Mg-calcite CCA in both high-CO2 (~ 700 ppm) and control (~ 380 ppm) environments, respectively. We reveal this stabilizing mechanism to be a combination of reduced porosity due to dolomite infilling and selective dissolution of other carbonate minerals. Physical break-up proceeds by dissolution of Mg-calcite walls until the dolomitized cell eventually drops out intact. Dolomite-rich CCA frameworks are common in shallow coral reefs globally and our results suggest that it is likely that they will continue to provide protection and stability for coral reef frameworks as CO2 rises.

Seawater carbonate chemistry and physiological responses of three temperate coralline algae in a laboratory experiment

Coralline algae are major calcifiers of significant ecological importance in marine habitats but are among the most sensitive calcifying organisms to ocean acidification. The elevated pCO2 effects were examined in three coralline algal species living in contrasting habitats from intertidal to subtidal zones on the north-western coast of Brittany, France: (i) Corallina elongata, a branched alga found in tidal rock pools, (ii) Lithophyllum incrustans, a crustose coralline alga from the low intertidal zone, and (iii) Lithothamnion corallioides (maerl), a free-living form inhabiting the subtidal zone. Metabolic rates were assessed on specimens grown for one month at varying pCO2: 380 (current pCO2), 550, 750 and 1000 µatm (elevated pCO2). There was no pCO2 effect on gross production in C. elongata and L. incrustans but L. incrustans respiration strongly increased with elevated pCO2. L. corallioides gross production slightly increased at 1000 µatm, while respiration remained unaffected. Calcification rates decreased with pCO2 in L. incrustans (both in the light and dark) and L. corallioides (only in the light), while C. elongata calcification was unaffected. This was consistent with the lower skeletal mMg/Ca ratio of C. elongata (0.17) relative to the two other species (0.20). L. incrustans had a higher occurrence of bleaching that increased with increasing pCO2. pCO2 could indirectly impact this coralline species physiology making them more sensitive to other stresses such as diseases or pathogens. These results underlined that the physiological response of coralline algae to near-future ocean acidification is species-specific and that species experiencing naturally strong pH variations were not necessarily more resistant to elevated pCO2 than species from more stable environment.

Growth response of an early successional assemblage of coralline algae and benthic diatoms to ocean acidification

The sustained absorption of anthropogenically released atmospheric CO2 by the oceans is modifying seawater carbonate chemistry, a process termed ocean acidification (OA). By the year 2100, the worst case scenario is a decline in the average oceanic surface seawater pH by 0.3 units to 7.75. The changing seawater carbonate chemistry is predicted to negatively affect many marine species, particularly calcifying organisms such as coralline algae, while species such as diatoms and fleshy seaweed are predicted to be little affected or may even benefit from OA. It has been hypothesized in previous work that the direct negative effects imposed on coralline algae, and the direct positive effects on fleshy seaweeds and diatoms under a future high CO2 ocean could result in a reduced ability of corallines to compete with diatoms and fleshy seaweed for space in the future. In a 6-week laboratory experiment, we examined the effect of pH 7.60 (pH predicted to occur due to ocean acidification just beyond the year 2100) compared to pH 8.05 (present day) on the lateral growth rates of an early successional, cold-temperate species assemblage dominated by crustose coralline algae and benthic diatoms. Crustose coralline algae and benthic diatoms maintained positive growth rates in both pH treatments. The growth rates of coralline algae were three times lower at pH 7.60, and a non-significant decline in diatom growth meant that proportions of the two functional groups remained similar over the course of the experiment. Our results do not support our hypothesis that benthic diatoms will outcompete crustose coralline algae under future pH conditions. However, while crustose coralline algae were able to maintain their presence in this benthic rocky reef species assemblage, the reduced growth rates suggest that they will be less capable of recolonizing after disturbance events, which could result in reduced coralline cover under OA conditions.

Effects of ocean acidification on population dynamics and community structure of crustose coralline algae

Calcification and growth of crustose coralline algae (CCA) are affected by elevated seawater pCO2 and associated changes in carbonate chemistry. However, the effects of ocean acidification (OA) on population and community-level responses of CCA have barely been investigated. We explored changes in community structure and population dynamics (size structure and reproduction) of CCA in response to OA. Recruited from an experimental flow-through system, CCA settled onto the walls of plastic aquaria and developed under exposure to one of three pCO2 treatments (control [present day, 389±6 ppm CO2], medium [753±11 ppm], and high [1267±19 ppm]). Elevated pCO2 reduced total CCA abundance and affected community structure, in particular the density of the dominant species Pneophyllum sp. and Porolithon onkodes. Meanwhile, the relative abundance of P. onkodes declined from 24% under control CO2 to 8.3% in high CO2 (65% change), while the relative abundance of Pneophyllum sp. remained constant. Population size structure of P. onkodes differed significantly across treatments, with fewer larger individuals under high CO2. In contrast, the population size structure and number of reproductive structures (conceptacles) per crust of Pneophyllum sp. was similar across treatments. The difference in the magnitude of the response of species abundance and population size structure between species may have the potential to induce species composition changes in the future. These results demonstrate that the impacts of OA on key coral reef builders go beyond declines in calcification and growth, and suggest important changes to aspects of population dynamics and community ecology.

Skeletal trade-offs in coralline algae in response to ocean acidification

Ocean acidification is changing the marine environment, with potentially serious consequences for many organisms. Much of our understanding of ocean acidification effects comes from laboratory experiments, which demonstrate physiological responses over relatively short timescales. Observational studies and, more recently, experimental studies in natural systems suggest that ocean acidification will alter the structure of seaweed communities. Here, we provide a mechanistic understanding of altered competitive dynamics among a group of seaweeds, the crustose coralline algae (CCA). We compare CCA from historical experiments (1981-1997) with specimens from recent, identical experiments (2012) to describe morphological changes over this time period, which coincides with acidification of seawater in the Northeastern Pacific. Traditionally thick species decreased in thickness by a factor of 2.0-2.3, but did not experience a change in internal skeletal metrics. In contrast, traditionally thin species remained approximately the same thickness but reduced their total carbonate tissue by making thinner inter-filament cell walls. These changes represent alternative mechanisms for the reduction of calcium carbonate production in CCA and suggest energetic trade-offs related to the cost of building and maintaining a calcium carbonate skeleton as pH declines. Our classification of stress response by morphological type may be generalizable to CCA at other sites, as well as to other calcifying organisms with species-specific differences in morphological types.

Phenotypic plasticity of coralline algae in a High CO2 world

It is important to understand how marine calcifying organisms may acclimatize to ocean acidification to assess their survival over the coming century. We cultured the cold water coralline algae, Lithothamnion glaciale, under elevated pCO2 (408, 566, 770, and 1024 µatm) for 10 months. The results show that the cell (inter and intra) wall thickness is maintained, but there is a reduction in growth rate (linear extension) at all elevated pCO2. Furthermore a decrease in Mg content at the two highest CO2 treatments was observed. Comparison between our data and that at 3 months from the same long-term experiment shows that the acclimation differs over time since at 3 months, the samples cultured under high pCO2 showed a reduction in the cell (inter and intra) wall thickness but a maintained growth rate. This suggests a reallocation of the energy budget between 3 and 10 months and highlights the high degree plasticity that is present. This might provide a selective advantage in future high CO2 world.

Nongeniculate coralline algae from IODP Site 310-M0005D

Material cored during the Integrated Ocean Drilling Program (IODP) Expedition 310 'Tahiti Sea Level' revealed that the fossil reef systems around Tahiti are composed of two major stratigraphic sequences: (i) a last deglacial sequence; and (ii) an older Pleistocene sequence. The older Pleistocene carbonate sequence is composed of reef deposits associated with volcaniclastic sediments and was preserved in Hole 310-M0005D drilled off Maraa. Within an approximately 70-m-thick older Pleistocene sequence (33.22-101.93 m below seafloor; 92.85-161.56 m below present sealevel) in this hole, 11 depositional units are defined by lithological changes, sedimentological features, and paleontological characteristics and are numbered sequentially from the top of the hole downward (Subunits P1-P11). Paleowater depths inferred from nongeniculate coralline algae, combined with those determined by using corals and larger foraminifers, suggest two major sealevel rises during the deposition of the older Pleistocene sequence. Of these, the second sealevel rise is associated with an intervening sealevel drop. It is likely that the second sealevel rise corresponds to that during Termination II (TII, the penultimate deglaciation, from Marine Isotope Stages 6 to 5e). Therefore, the intervening sealevel drop can be correlated with that known as the 'sealevel reversal' during TII. Because there are limited data on the Pleistocene reef systems in the tropical South Pacific Ocean, this study provides important information about Pleistocene sealevel history, the evolution of coral reef ecosystems, and the responses of coral reefs to Quaternary climate changes.

Seawater carbonate chemistry and settlement of a spawning coral on three common species of crustose coralline algae

Concern about the impacts of ocean acidification (OA) on ecosystem function has prompted many studies to focus on larval recruitment, demonstrating declines in settlement and early growth at elevated CO2 concentrations. Since larval settlement is often driven by particular cues governed by crustose coralline algae (CCA), it is important to determine whether OA reduces larval recruitment with specific CCA and the generality of any effects. We tested the effect of elevated CO2 on the survival and settlement of larvae from the common spawning coral Acropora selago with 3 ecologically important species of CCA, Porolithon onkodes, Sporolithon sp., and Titanoderma sp. After 3 d in no-choice laboratory assays at 447, 705, and 1214 µatm pCO2, the rates of coral settlement declined as pCO2 increased with all CCA taxa. The magnitude of the effect was highest with Titanoderma sp., decreasing by 87% from the ambient to highest CO2 treatment. In general, there were high rates of larval mortality, which were greater with the P. onkodes and Sporolithon sp. treatments (~80%) compared to the Titanoderma sp. treatment (65%). There was an increase in larval mortality as pCO2 increased, but this was variable among the CCA species. It appears that OA reduces coral settlement by rapidly altering the chemical cues associated with the CCA thalli and microbial community, and potentially by directly affecting larval viability.