Crustose Coralline Red Algae Research Articles

Editorial: Crustose coralline red algae frameworks and rhodoliths: Past and present

Editorial: Crustose coralline red algae frameworks and rhodoliths: Past and present

Video survey of deep benthic macroalgae and macroalgal detritus along a glacial Arctic fjord: Kongsfjorden (Spitsbergen)

In Kongsfjorden (Spitsbergen), we quantified the zonation of visually dominant macroalgal taxa and of detached macroalgae from underwater videos taken in summer 2009 at six transects between 2 and 138 m water depth. For the first time, we provide information on the occurrence of deep water red algae below the kelp forest and of detached macroalgae at water depth > 30 m. The presence and depth distribution of visually dominant red algae were especially pronounced at the outer fjord, decreased with proximity to the glacial front and they were absent at the innermost locations. Deepest crustose coralline red algae and foliose red algae were observed at 72 and 68 m, respectively. Brown algae were distributed along the entire fjord axis at 2–32 m. Green algae were only present at the middle to inner fjord and at areas influenced by physical disturbance at water depths of 2–26 m. With proximity to the inner fjord the depth distribution of all macroalgae became shallower and only extended to 18 m depth at the innermost location. Major recipients of detached macroalgae were sites at the shallower inner fjord and at the middle fjord below the photic zone at depths to 138 m. They may either fuel deep water secondary production, decompose or support carbon sequestration. Univariate and community analyses of macroalgal classes including detached macroalgae across transects and over depths reveal a considerable difference in community structure between the outermost sites, the central part and the inner fjord areas, reflecting the strong environmental gradients along glacial fjords.

Calcium carbonate production in the southernmost subtropical Atlantic coral reef

Emerging evidence have been supporting the idea that the better known South Atlantic coral reefs (located between 18°S and 24°S) are now essentially senescent structures that have experienced little or no additional vertical reef growth over the past millennia. This has often coincided with a shift to a dominance of non-coral calcifying organisms becoming the main CaCO3 producers in these high latitude and marginal marine settings. Here, we used Calcification Accretion Units (CAUs) and census-based methods to measure non-coral rates of CaCO3 production on the geologically senescent reef and adjacent rhodolith beds within the southernmost subtropical Atlantic reef (i.e., Queimada Grande Reef, QGR). The reef habitat is currently producing CaCO3 at rates of ∼126 g m−2 yr−1. In contrast, fragments of dead corals skeletons deposited adjacent to the reef over the last ∼2000 years are now colonized by crustose coralline red algae. These form a rhodolith bed that produces CaCO3 at rates of 858 g m−2 yr−1. Our results indicate that, whilst not sufficient to promote active net framework accumulation, CaCO3 production by coralline algae and bryozoans on the QGR appears to be sufficient to at least limit net large-scale erosion of the underlying reef structure, allowing the reef structure to persist in a state close to budgetary stasis. Finally, our results are also of relevance for providing insights regarding the balance of CaCO3 production/dissolution/erosion processes in coral reefs, especially in these less understood marginal reefs.

A possible link between coral reef success, crustose coralline algae and the evolution of herbivory

Crustose coralline red algae (CCA) play a key role in the consolidation of many modern tropical coral reefs. It is unclear, however, if their function as reef consolidators was equally pronounced in the geological past. Using a comprehensive database on ancient reefs, we show a strong correlation between the presence of CCA and the formation of true coral reefs throughout the last 150 Ma. We investigated if repeated breakdowns in the potential capacity of CCA to spur reef development were associated with sea level, ocean temperature, CO2 concentration, CCA species diversity, and/or the evolution of major herbivore groups. Model results show that the correlation between the occurrence of CCA and the development of true coral reefs increased with CCA diversity and cooler ocean temperatures while the diversification of herbivores had a transient negative effect. The evolution of novel herbivore groups compromised the interaction between CCA and true reef growth at least three times in the investigated time interval. These crises have been overcome by morphological adaptations of CCA.

Disease Specific Bacterial Communities in a Coralline Algae of the Northwestern Mediterranean Sea: A Combined Culture Dependent and -Independent Approach.

Crustose coralline red algae (CCA) are important components of marine ecosystems thriving from tropical waters and up to the poles. They fulfill important ecological services including framework building and induction of larval settlement. Like other marine organisms, CCAs have not been spared by the increase in marine disease outbreaks. The white-band syndrome has been recently observed in corallines from the Mediterranean Sea indicating that the disease threat has extended from tropical to temperate waters. Here, we examined the microbiome and the pathobiome of healthy and diseased Neogoniolithon brassica-florida coralline algae in the Mediterranean Sea by combining culture-dependent and -independent approaches. The coralline white-band syndrome was associated with a distinct pathobiome compared to healthy tissues and showed similarities with the white-band syndrome described in the Caribbean Sea. A sequence related to the genus Hoeflea, order Rhizobiales, characterized the white-band disease pathobiome described by amplicon sequencing. No representative of this genus was isolated by culture. We, however, successfully isolated an abundant member of the healthy CCA microbiome, an Alphaproteobateria of the family Rhodobacteraceae. In conclusion, we did not identify a potential causative agent of the disease, but through the complementarity of culture dependent and independent approaches we characterized the healthy microbiome of the coralline and the possible opportunistic bacteria colonizing diseased tissues.

Calibration of the pH-δ11B and temperature-Mg/Li proxies in the long-lived high-latitude crustose coralline red alga Clathromorphum compactum via controlled laboratory experiments

A solid understanding of global oceanic change throughout Holocene time is needed to contextualize and interpret recent observations of rapid warming (Moore, 2016), ocean acidification (Popova et al., 2014; Qi et al., 2017), increasing meltwater input (Halfar et al., 2013; Notz and Stroeve, 2016) and circulation changes (Liu et al., 2017; Rahmstorf et al., 2015; Yang et al., 2016) in the Arctic and subarctic Oceans. Precisely reconstructing acidification and temperature variations throughout the Holocene will provide a vital context for interpreting current environmental changes and future climate projections in the region. However, existing paleoenvironmental reconstructions are sparse and uncertain, largely owing to limited availability of high fidelity paleoceanographic archives, such as marine carbonates, in high latitude waters. Coralline algae of the genus Clathromorphum have emerged as key candidates for reconstructing high-latitude environmental variability at annual to sub-annual resolution. Here, we present the first empirical calibrations of boron isotope-pH and Mg/Li-temperature relationships within the long-lived, crustose coralline red alga Clathromorphum compactum. Calibration experiments were performed in triplicate, growing wild-collected specimens for four months at three controlled temperatures (6.4 – 12.4 oC) and four pCO2 conditions (352 - 3230 ppm), to test the effects of these environmental parameters on the isotopic and elemental composition of the algal skeleton. We find that boron isotopes within the skeleton of C. compactum (δ11Bcc) are well correlated with δ11B of seawater borate (δ11Βborate), defining the following equation: δ11Βcc (2σ) = 1.46 (0.06) δ11Βborate + 6.91 (0.72). This equation can be used to reconstruct δ11Βborate of the coralline alga’s ambient seawater, from which past seawater pH can be calculated. We also identified a strong correlation between skeletal Mg/Li ratio and seawater temperature, defined by the equation: Mg/Li (2σ) = 0.17 (0.02) temperature (oC) + 1.02 (0.16). Therefore, despite the strong biological control that this species appears to exert on calcification site pH (elevated 1.0-1.6 pH units above seawater pH, inferred from δ11Bcc > δ11Βborate), and the apparent relationship between skeletal extension rate and skeletal Li/Ca and Mg/Ca, the δ11Bcc and Mg/Li ratios of the coralline alga’s skeleton strongly and significantly respond to ambient seawater pH and temperature, respectively. These results support the use of δ11B and Mg/Li within C. compactum for pH and temperature reconstructions of northern high-latitude oceans.

Occurrence of Live Rhodolith Bed of <i>Lithophyllum kotschyanum</i> Unger (Corallinaceae:Lithophylloideae) in Palk Bay:First Record from India

Rhodoliths are nodular form of marine free-living, non-geniculate, crustose coralline red algae, resembling the corals. The communities, in which they dominate are referred to as ‘rhodolith beds’, ‘rhodolites’ or ‘maerl’. Rhodoliths assume different sizes, shapes and forms (small thalli-like, twig-like, large round shaped, branching/unbranching, etc.) based on different factors such as water motion, bioturbation, grazing, fouling, bleaching, etc..

Eukaryotic Life Inhabits Rhodolith-forming Coralline Algae (Hapalidiales, Rhodophyta), Remarkable Marine Benthic Microhabitats

Rhodoliths are benthic calcium carbonate nodules accreted by crustose coralline red algae which recently have been identified as useful indicators of biomineral changes resulting from global climate change and ocean acidification. This study highlights the discovery that the interior of rhodoliths are marine biodiversity hotspots that function as seedbanks and temporary reservoirs of previously unknown stages in the life history of ecologically important dinoflagellate and haptophyte microalgae. Whereas the studied rhodoliths originated from offshore deep bank pinnacles in the northwestern Gulf of Mexico, the present study opens the door to assess the universality of endolithic stages among bloom-forming microalgae spanning different phyla, some of public health concerns (Prorocentrum) in marine ecosystems worldwide.

Aragonite infill in overgrown conceptacles of coralline Lithothamnion spp. (Hapalidiaceae, Hapalidiales, Rhodophyta): new insights in biomineralization and phylomineralogy.

New empirical and quantitative data in the study of calcium carbonate biomineralization and an expanded coralline psbA framework for phylomineralogy are provided for crustose coralline red algae. Scanning electron microscopy (SEM) and energy dispersive spectrometry (SEM-EDS) pinpointed the exact location of calcium carbonate crystals within overgrown reproductive conceptacles in rhodolith-forming Lithothamnion species from the Gulf of Mexico and Pacific Panama. SEM-EDS and X-ray diffraction (XRD) analysis confirmed the elemental composition of these calcium carbonate crystals to be aragonite. After spore release, reproductive conceptacles apparently became overgrown by new vegetative growth, a strategy that may aid in sealing the empty conceptacle chamber, hence influencing the chemistry of the microenvironment and in turn promoting aragonite crystal growth. The possible relevance of various types of calcium carbonate polymorphs present in the complex internal structure and skeleton of crustose corallines is discussed. This is the first study to link SEM, SEM-EDS, XRD, Microtomography and X-ray microscopy data of aragonite infill in coralline algae with phylomineralogy. The study contributes to the growing body of literature characterizing and speculating about how the relative abundances of carbonate biominerals in corallines may vary in response to changes in atmospheric pCO2 , ocean acidification, and global warming.

SUBARCTIC RHODOLITH BEDS PROMOTE LONGEVITY OF CRUSTOSE CORALLINE ALGAL BUILDUPS AND THEIR CLIMATE ARCHIVING POTENTIAL

ABSTRACT The rocky, photic benthos of Arctic and Subarctic Biogeographic Regions has a characteristic seaweed flora that includes an extensive high-magnesium calcium carbonate basal layer of crustose coralline red algae. The thickest (10–40 cm) and oldest parts of the crust (previously reported as up to 640–830 years old), primarily at mid-photic depths of 15–25 m, are composed of buildups of the genus Clathromorphum. Due to its annual growth increments and cycling of Mg content with temperature, Clathromorphum has recently been developed as a high-resolution climate archive. The age of the archive is primarily limited by the boring of mollusks that reduce structural integrity, remove the record, and induce local diagenesis. Depressions and gentle slopes in the deeper portions of Subarctic rocky bottoms often collect mixed bioclastic and siliciclastic sediments, including a dense cover of rhodoliths (Lithothamnion glaciale and Lithothamnion tophiforme). In this paper we describe a transition zone of these...

Morphology of the crustose coralline alga Pseudolithophyllum muricatum (Corallinales, Rhodophyta) responds to 30years of ocean acidification in the Northeast Pacific.

As the process of ocean acidification alters seawater carbon chemistry, physiological processes such as skeletal accretion are expected to become more difficult for calcifying organisms. The crustose coralline red algae (Corallinales, Rhodophyta) form an important guild of calcifying primary producers in the temperate Northeast Pacific. The morphology of important ecological traits, namely, skeletal density and thallus thickness near the growing edge, was evaluated in Pseudolithophyllum muricatum (Foslie) Steneck & R.T. Paine, the competitively dominant alga within this guild. P.muricatum shows a morphological response to increased ocean acidification in the temperate Northeast Pacific. Comparing historical (1981-1997) and modern (2012) samples from the field, crust thickness near the growing edge was approximately half as thick in modern samples compared with historical samples, while crust calcite density showed no significant change between the two sample groups. Morphological changes at the growing edge have important consequences for mediating competitive interactions within this guild of algae, and may affect the role of crustose coralline algal beds as hosts to infaunal communities and facilitators of recruitment in many invertebrate and macroalgal species.

Succession of crustose coralline red algae (Rhodophyta) on coralgal reefs exposed to physical disturbance in the southwest Atlantic

Biological and physical disturbances create the conditions for species succession in any biological ecosystem. In particular, coral reefs are susceptible to this process because of the complexity of their ecological relationships. In the southwest Atlantic, nearshore reefs are mostly coated by a thin layer of coralline crusts rather than stony corals. However, little is known about the succession of crustose coralline algae. We studied this process by means of a series of experimental and control discs exposed to physical disturbance. Our results showed that the dominant species in natural conditions, Pneophyllum conicum, had early recruits and later became dominant on the discs, replicating the community structure of the actual reef. This species had mature reproductive structures and available spores from the beginning of the colonization experiments. Thicker crusts of Porolithon pachydermum and Peyssonnelia sp. were found on the discs after 112 days, and significantly increased their cover over the succeeding months; and after 1 year, P. conicum was less abundant. Physical disturbance increased crust recruitment and the low-light environment created by sediments. The data demonstrated coexistence among crustose coralline species and a tolerance to physical disturbance, which seemed to favor the thinner crusts of P. conicum over thick-crust species during succession. The succession pattern observed in this subtropical Brazilian coral reef differs from that described for shallow tropical reef communities.

Calcification of the Arctic coralline red algae Lithothamnion glaciale in response to elevated CO2

Rising atmospheric CO2 concentrations could cause a calcium carbonate subsaturation of Arctic surface waters in the next 20 yr, making these waters corrosive for calcareous organisms. It is presently unknown what effects this will have on Arctic calcifying organisms and the ecosystems of which they are integral components. So far, acidification effects on crustose coralline red algae (CCA) have only been studied in tropical and Mediterranean species. In this work, we investigated calcification rates of the CCA Lithothamnion glaciale collected in northwest Svalbard in laboratory experiments under future atmospheric CO2 concentrations. The algae were exposed to simulated Arctic summer and winter light conditions in 2 separate experiments at optimum growth temperatures. We found a significant negative effect of increased CO2 levels on the net calcification rates of L. glaciale in both experiments. Annual mean net dissolution of L. glaciale was estimated to start at an aragonite saturation state between 1.1 and 0.9 which is projected to occur in parts of the Arctic surface ocean between 2030 and 2050 if emissions follow ‘business as usual’ scenarios (SRES A2; IPCC 2007). The massive skeleton of CCA, which consist of more than 80% calcium carbonate, is considered crucial to withstanding natural stresses such as water movement, overgrowth or grazing. The observed strong negative response of this Arctic CCA to increased CO2 levels suggests severe threats of the projected ocean acidification for an important habitat provider in the Arctic coastal ocean.

Rhodolith transport and immobilization on a volcanically active rocky shore: Middle Miocene at Cabeço das Laranjas on Ilhéu de Cima (Madeira Archipelago, Portugal)

Extraordinary deposits of fossil rhodoliths occur at the Cabeço das Laranjas (Portuguese~Hill of the Oranges) in a small fault block at the northwest end of Ilhéu de Cima off Porto Santo in the Madeira Archipelago. Stratigraphic repetitions of densely packed rhodolith beds up to 2.6m thick are associated with a receding rocky shoreline, and are interpreted as the result of hurricanes. The initial storm deposit sits unconformably on basalt and eroded basalt boulders associated with tuff and volcaniclastic breccia. Approximately 90,000 rhodoliths of Middle Miocene age (14–15Ma) are exposed on the upper surface of the initial deposit over a 450-m2 shelf exhumed from the hill's southeast side. Ranging in diameter from ≤3cm to 20cm, many of the rhodoliths generated by crustose coralline red algae are now iron stained and resemble a mass of oranges in gross appearance. Sea stacks and large boulders rise through the thick basal rhodolith bed to form small catchment areas that held the deposit in place after the storm's passage. The succeeding rhodolith deposits are variably separated by layers with mixed carbonate and volcanic sand, pure volcanic lapilli, and volcaniclastic tephra mixed with tuff showing swaley cross-stratification. Three out of four rhodolith beds are truncated against the flank of the adjoining rocky shore. Only the youngest (fourth) rhodolith layer is fully exposed around the perimeter of the hill and can be shown to cross a basalt barrier that is traceable for 70m in cross section as an erosional ramp dipping from 6° to 8° southeast. The entire fossil-rich sequence is capped by a basalt flow showing columnar disjunction. Based on thin-section analysis, three genera of coralline red algae are recognized in the basal rhodolith deposit: Sporolithon, Lithothamnion, and Neogoniolithon. Associated biodiversity is low, represented by 16 kinds of marine invertebrates dominated by encrustations and borings on the rhodoliths and very few free body fossils. The Madeira region of the North Atlantic may have been susceptible to major cyclonic storms immediately after the Middle Miocene Climate Optimum, when a northward shift of the Inter-tropical Convergence Zone was stimulated by a steeper temperature gradient in the southern hemisphere related to expansion of continental glaciers on Antarctica.

Marine biological community baselines in unimpacted tropical ecosystems: spatial and temporal analysis of reefs at Howland and Baker Islands

Howland and Baker Islands are two small, isolated reef and sand islets located near the equator in the central Pacific Ocean that are situated approximately 60 km apart. In 2004 and 2006, species-level monitoring at multiple sites, coupled with towed-diver surveys in 2002, 2004, and 2006 on both of these federally protected islands, revealed diverse fish, coral, macroinvertebrate, and algal assemblages. This study examines inter- and intra-island spatial and temporal differences in community composition among sites and presents baseline biological community parameters for two of the least impacted reef systems in the world. Despite similarities in species composition, permutational multivariate analysis of variance (PERMANOVA) and multidimensional scaling ordinations (nMDS) suggest biological communities at the two islands are distinct with Baker Island containing a greater percent cover of branched Acroporid corals and turf algae and Howland Island containing a greater percent cover of crustose coralline red algae and small, compact genera of coral. Both islands also contained considerable cover of non-invasive macroalgae. PERMANOVA further revealed benthic and fish species composition to differ between forereef and reef shelf sites from different sides of each island. When islands were considered as a whole, temporal changes were not noted between 2004 and 2006; however, temporal changes at select sites did occur, with coral cover decreasing significantly along the west side of Baker Island from 2004 to 2006.

Coralline alga reveals first marine record of subarctic North Pacific climate change

While recent changes in subarctic North Pacific climate had dramatic effects on ecosystems and fishery yields, past climate dynamics and teleconnection patterns are poorly understood due to the absence of century‐long high‐resolution marine records. We present the first 117‐year long annually resolved marine climate history from the western Bering Sea/Aleutian Island region using information contained in the calcitic skeleton of the long‐lived crustose coralline red alga Clathromorphum nereostratum, a previously unused climate archive. The skeletal δ18O‐time series indicates significant warming and/or freshening of surface waters after the middle of the 20th century. Furthermore, the time series is spatiotemporally correlated with Pacific Decadal Oscillation (PDO) and tropical El Niño‐Southern Oscillation (ENSO) indices. Even though the western Bering Sea/Aleutian Island region is believed to be outside the area of significant marine response to ENSO, we propose that an ENSO signal is transmitted via the Alaskan Stream from the Eastern North Pacific, a region of known ENSO teleconnections.

Temporal and spatial comparison of the relative abundance of macroalgae across the Mariana Archipelago between 2003 and 2005

A.D. Tribollet and P.S. Vroom. 2007. Temporal and spatial comparison of the relative abundance of macroalgae across the Mariana Archipelago between 2003 and 2005. Phycologia 46: 187–197. DOI: 10.2216/06-46.1Past studies have argued that macroalgae serve as useful bioindicators that herald possible environmental changes to reef ecosystems because they are often opportunistic, having high growth rates and responding quickly to environmental changes, such as increased nutrient availability, grazing pressures, or storm activity. In this study, we test their usefulness as reef monitoring management indicators. We investigated the spatial and temporal variability of the relative abundance of macroalgae (RAM) at the genus level in the Mariana Archipelago between two surveys in 2003 and 2005. Islands vary drastically across the archipelago (carbonate vs volcanic, populated vs unpopulated, small vs large) and often experience considerable storm activity. We showed that the diversity of macroalgal genera was generally highest at the southern end of the archipelago, probably because of increased habitat heterogeneity around these geographically larger islands. At the northern end of the archipelago, only Pagan and Maug were large enough or contained enough environmental diversity to exhibit macroalgal diversity similar to that of the southern carbonate islands. Despite the ubiquitous nature of turf algae, crustose coralline red algae, and the green alga Halimeda (Bryopsidales) across the archipelago, multivariate analyses revealed RAM to differ among islands with northern, unpopulated, volcanic islands grouping together and differing from southern, populated, carbonate islands. Also, RAM showed significant variability at the local scale (among sites within an island) and over time. We hypothesize that this variability results principally from differing oceanographic conditions such as sea surface temperature, human impacts such as fishing and pollution, typhoons, and volcanic activity across the archipelago. These results provide a baseline for future monitoring studies in the Mariana Archipelago and suggest that rapid ecological assessments of macroalgae in the field at the genus level are a reliable indicator that can be used to monitor change over time.

10 サンゴ幼生に作用する無節サンゴモの他感作用物質(口頭発表の部)

10 サンゴ幼生に作用する無節サンゴモの他感作用物質(口頭発表の部)

Characterization of a natural inducer of coral larval metamorphosis

External chemical signals used by scleractinian corals to recognize suitable substrata for larval settlement and metamorphosis were identified from crustose coralline red algae (CCA). A fragment of coral rubble with CCA induced larval metamorphosis of the scleractinian coral Pseudosiderastrea tayamai. A natural inducer and compounds that enhanced its effect in larval metamorphosis were isolated from the methanol extracts of coral rubble with CCA. A bromotyrosine derivative, 11-deoxyfistularin-3 (10 − 7 M) isolated from the CCA, induced the metamorphosis of P. tayamai larvae (27.5 ± 24.0%). In the presence of fucoxanthinol (10 − 9 M) and fucoxanthin (10 − 9 M), the percentage of metamorphosis induced by the bromotyrosine derivative was further enhanced to 87.8 ± 13.0 and 88.4 ± 17.8%, respectively. Both carotenoids are also found in the coral rubble with CCA. These results suggest that bromotyrosine derivative and carotenoids have a synergistic effect in the metamorphosis of P. tayamai larvae. The synergistic effect provides a higher selectivity for recruitment than a single-component natural inducer for recognizing suitable substrata for larval metamorphosis. Thus, the effect might offer a survival advantage for benthic marine invertebrates.

Corallinafuran and Corallinaether, Novel Toxic Compounds from Crustose Coralline Red Algae.

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