Phylogenetic analysis of rhodolith formation in the Corallinales (Rhodophyta)

Although the ecological importance of rhodolith (maerl, free-living coralline algae) beds is well-known, rhodolith-forming species have been neglected in molecular phylogenetic studies. This is the first molecular systematic study aimed at understanding whether the rhodolith habit is a fixed feature in lineages and determining the relationship (phylogenetic vs. environmental) between rhodolith and crustose habits. Phylogenetic relationships of rhodolith-forming species and encrusting coralline algae at generic and species levels were analysed using SSU rDNA and psbA sequences. Extensive sampling in the European North Atlantic, Pacific and Caribbean Mexico of Phymatolithon, Lithothamnion, Lithophyllum and Neogoniolithon taxa forming rhodoliths and crusts was accompanied by examination of type or topotype material. Phylogenetic reconstruction showed that Neogoniolithon contained a monophyletic group of rhodolith-forming species whereas other rhodolith-formers were closely related to encrusting forms in the genera Phymatolithon, Lithothamnion, Mesophyllum, Hydrolithon, Spongites and Sporolithon. DNA analysis showed that the crust-forming Lithophyllum cf. incrustans/dentatum also forms rhodoliths with a stone nucleus that occur on rocky shores. In contrast, species that form beds of non-nucleate rhodoliths (e.g. Neogoniolithon spectabile, N. strictum, Lithophyllum cf. incrustans/dentatum or sp. 1 and Phymatolithon calcareum) rarely form crusts. The rhodolith habit cannot be used to delimit species for taxonomic or identification purposes. Extensive taxonomic revision will be required to deal with problems such as the position of specimens identified as Lithophyllum margaritae in two unrelated lineages.     

New records of rhodolith-forming species (Corallinales, Rhodophyta) from deep water in Espírito Santo State, Brazil

Little is known about the diversity of non-geniculate coralline red algae (Rhodophyta, Corallinophycidae) from deep waters in Brazil. Most surveys undertaken in this country have been carried out in shallow waters. In 1994, however, the REVIZEE program surveyed the sustainable living resources potential of the Brazilian exclusive economic zone to depths of 500?m. In the present study, the rhodolith-forming coralline algae from the continental shelf of Espírito Santo State were identified. Samples were taken from 54 to 60?m depth by dredging during ship cruises in 1997. Three rhodolith-forming species were found: Spongites yendoi (Foslie) Chamberlain, Lithothamnion muelleri Lenormand ex Rosanoff and Lithothamnion glaciale Kjellman. These records extend the distribution ranges of these species into Brazilian waters and extend the depth distribution of non-geniculate coralline red algae into Brazilian water to 58?m.     

ANALYSIS OF ANCIENT DNA FROM FOSSIL CORALLINES (CORALLINALES,RHODOPHYTA)1

The field of molecular paleontology has recently made significant contributions to anthropology and biology. Hundreds of ancient DNA studies have been published, but none has targeted fossil coralline algae. Using regions of the SSU gene, we analyzed rDNA from fossil coralline algae of varying ages and states of preservation from Spain, Papua New Guinea (PNG), and the Great Barrier Reef (GBR). Specimens from PNG, GBR, and some localities from Spain did not contain endogenous ancient DNA. Reproducible sequence data were obtained from specimens ～550 years old from near Cadiz, Spain, and from rocky‐shore deposits in Carboneras, Almeria Province of Spain (～78,000 years before present [YBP]). Based on BLAST searches and a phylogenetic analysis of sequences, an undescribed coralline alga belonging to the Melobesioideae was discovered in the Carboneras material as well as the following coralline genera: Jania, Lithophyllum, Lithothamnion, Mesophyllum, and Phymatolithon. DNA from fleshy brown and red macroalgae was also discovered in the specimens from Carboneras. The coralline algae identified using molecular techniques were in agreement with those based on morphological methods. The identified taxa are common in the present‐day southeastern Spain littoral zone. Amino acid racemization, concentration ratios, and specific concentrations failed to show a correlation between biomolecular preservation and PCR amplification success. Results suggest that molecular investigations on fossil algae, although limited by technical difficulties, are feasible. Validity of our results was established using authentication criteria and a self‐critical approach to compliance.     

Establishing temperate crustose early Holocene coralline algae as archives for palaeoenvironmental reconstructions of the shallow water habitats of the Mediterranean Sea

Over the past decades, coralline algae have increasingly been used as archives of palaeoclimate information due to their seasonal growth bands and their vast distribution from high latitudes to the tropics. Traditionally, these reconstructions have been performed mainly on high latitude species, limiting the geographical area of their potential use. Here we assess the use of temperate crustose fossil coralline algae from shallow water habitats for palaeoenvironmental reconstruction to generate records of past climate change. We determine the potential of three different species of coralline algae, Lithothamnion minervae, Lithophyllum stictaeforme and Mesophyllum philippii, with different growth patterns, as archives for pH (δ¹¹B) and temperature (Mg/Ca) reconstruction in the Mediterranean Sea. Mg concentration is driven by temperature but modulated by growth rate, which is controlled by species-specific and intraspecific growth patterns. L. minervae is a good temperature recorder, showing a moderate warming trend in specimens from 11.37 cal ka BP (from 14.2 ± 0.4°C to 14.9 ± 0.15°C) to today. In contrast to Mg, all genera showed consistent values of boron isotopes (δ¹¹B) suggesting a common control on boron incorporation. The recorded δ¹¹B in modern and fossil coralline specimens is in agreement with literature data about early Holocene pH, opening new perspectives of coralline-based, high-resolution pH reconstructions in deep time.     

Coralline algae as depth indicators in the Sommières Basin (early Miocene,Southern France)

The aim of this work is to demonstrate the benefits of digital surface-quantification and species identification in the study of coralline algae. Within the well-constrained context of the Miocene Sommières Basin (Southern France), whose sedimentological and paleontological setting has been reconstructed by previous researches, the abundance of coralline algae is estimated through quantification of the area occupied by the different species, which are thoroughly described in order to make future taxonomic-revisions as easy as possible. Coralline distribution patterns are studied along a bathymetric gradient to assess the response of the major groups and of the different species to variations in water depth. Surface quantification highlights clear trends both at the species level and higher taxonomic ranks, showing that coralline algae can be a quite accurate instrument in paleoenvironmental reconstructions. Among the clearly identified species, Lithophyllum sp. A, Sporolithon sp. A, and Spongites fruticulosus prefer shallow-water; Mesophyllum roveretoi dominates at intermediate depth together with Lithothamnion ponzonense, while Phymatolithon sp. A occurs at the lower limit of the photic zone. The approach presented here can be applied to a variety of different contexts, providing a powerful instrument for the interpretation of coralline-algal associations.     

AN SEM‐BASED ANALYSIS OF THE MORPHOLOGY,ANATOMY, AND REPRODUCTION OF LITHOTHAMNION TOPHIFORME (ESPER) UNGER (CORALLINALES,RHODOPHYTA), WITH A COMPARATIVE STUDY OF ASSOCIATED NORTH ATLANTIC ARCTIC/SUBARCTIC MELOBESIOIDEAE1

Lithothamnion tophiforme (Esper) Unger is a dominant, arctic, saxicolous species that extends southward, albeit with reduced cover, into the deeper colder waters of the North Atlantic subarctic, where it also occurs in significant rhodolith deposits with L. glaciale. The external appearance of L. tophiforme is distinctive, but typification, anatomy, reproduction, ecology, and biogeography have not been previously analyzed. These topics are now addressed, with extensive use of SEM, in comparison with other North Atlantic arctic and subarctic melobesioid genera and species. The species considered in this article comprise 95% of the coralline biomass of the colder North Atlantic and adjacent arctic (i.e. less than 12° C summer and less than 0° C winter). In the outer thallus region of coralline algae, crust extension proceeds, calcification develops, surface sloughing and grazing occur, and reproductive structures are initiated. Analysis of the ultrastructure of the outer thallus region (epithallium, meristem, and perithallium) of L. tophiforme shows distinctive generic similarities and specific differences from the other Lithothamnion species discussed here. Considerable generic differences from the Clathromorpum and Leptophytum species also encountered in the region considered are highlighted as well. We discuss the functional and taxonomic implications of these distinguishing features and recommend that they be more widely considered in future research on coralline algae to understand more fully the ecology and evolution of the Corallinales.     

A Multilocus Species Delimitation Reveals a Striking Number of Species of Coralline Algae Forming Maerl in the OSPAR Maritime Area

Maerl beds are sensitive biogenic habitats built by an accumulation of loose-lying, non-geniculate coralline algae. While these habitats are considered hot-spots of marine biodiversity, the number and distribution of maerl-forming species is uncertain because homoplasy and plasticity of morphological characters are common. As a result, species discrimination based on morphological features is notoriously challenging, making these coralline algae the ideal candidates for a DNA barcoding study. Here, mitochondrial (COI-5P DNA barcode fragment) and plastidial (psbA gene) sequence data were used in a two-step approach to delimit species in 224 collections of maerl sampled from Svalbard (78°96’N) to the Canary Islands (28°64’N) that represented 10 morphospecies from four genera and two families. First, the COI-5P dataset was analyzed with two methods based on distinct criteria (ABGD and GMYC) to delineate 16 primary species hypotheses (PSHs) arranged into four major lineages. Second, chloroplast (psbA) sequence data served to consolidate these PSHs into 13 secondary species hypotheses (SSHs) that showed biologically plausible ranges. Using several lines of evidence (e.g. morphological characters, known species distributions, sequences from type and topotype material), six SSHs were assigned to available species names that included the geographically widespread Phymatolithon calcareum, Lithothamnion corallioides, and L. glaciale; possible identities of other SSHs are discussed. Concordance between SSHs and morphospecies was minimal, highlighting the convenience of DNA barcoding for an accurate identification of maerl specimens. Our survey indicated that a majority of maerl forming species have small distribution ranges and revealed a gradual replacement of species with latitude.     

Biomineralization of calcium carbonate in the cell wall of Lithothamnion crispatum (Hapalidiales,Rhodophyta): correlation between the organic matrix and the mineral phase

Over the past few decades, progress has been made toward understanding the mechanisms of coralline algae mineralization. However, the relationship between the mineral phase and the organic matrix in coralline algae has not yet been thoroughly examined. The aim of this study was to describe the cell wall ultrastructure of Lithothamnion crispatum, a cosmopolitan rhodolith‐forming coralline algal species collected near Salvador (Brazil), and examine the relationship between the organic matrix and the nucleation and growth/shape modulation of calcium carbonate crystals. A nanostructured pattern was observed in L. crispatum along the cell walls. At the nanoscale, the crystals from L. crispatum consisted of several single crystallites assembled and associated with organic material. The crystallites in the bulk of the cell wall had a high level of spatial organization. However, the crystals displayed cleavages in the (104) faces after ultrathin sectioning with a microtome. This organism is an important model for biomineralization studies as the crystallographic data do not fit in any of the general biomineralization processes described for other organisms. Biomineralization in L. crispatum is dependent on both the soluble and the insoluble organic matrix, which are involved in the control of mineral formation and organizational patterns through an organic matrix‐mediated process. This knowledge concerning the mineral composition and organizational patterns of crystals within the cell walls should be taken into account in future studies of changing ocean conditions as they represent important factors influencing the physico‐chemical interactions between rhodoliths and the environment in coralline reefs.     

Misleading morphologies and the importance of sequencing type specimens for resolving coralline taxonomy (Corallinales,Rhodophyta): Pachyarthron cretaceum is Corallina officinalis

Coralline red algae play a key role in the ecology of near shore marine ecosystems and are increasingly being used to study the effects of climate change in the marine environment. Corallines are very difficult to identify to species, and even to genus, using morpho‐anatomy, likely complicating studies of their ecology, physiology, and biodiversity. We sequenced a 296 base pair fragment of chloroplast DNA from a 187‐year‐old isolectotype specimen of Pachyarthron cretaceum, a morphologically distinct geniculate species, to demonstrate that coralline morphology is often misleading and that species names can only be applied unequivocally by comparing DNA sequences from type material with sequences from field‐collected specimens. Our results indicate that Pachyarthron cretaceum is synonymous with Corallina officinalis.     

New branched Porolithon species (Corallinales,Rhodophyta) from the Great Barrier Reef,Coral Sea,and Lord Howe Island

Porolithon is one of the most ecologically important genera of tropical and subtropical crustose (non-geniculate) coralline algae growing abundantly along the shallow margins of coral reefs and functioning to cement reef frameworks. Thalli of branched, fruticose Porolithon specimens from the Indo-Pacific Ocean traditionally have been called P. gardineri, while massive, columnar forms have been called P. craspedium. Sequence comparisons of the rbcL gene both from type specimens of P. gardineri and P. craspedium and from field-collected specimens demonstrate that neither species is present in east Australia and instead resolve into four unique genetic lineages. Porolithon howensis sp. nov. forms columnar protuberances and loosely attached margins and occurs predominantly at Lord Howe Island; P. lobulatum sp. nov. has fruticose to clavate forms and free margins that are lobed and occurs in the Coral Sea and on the Great Barrier Reef (GBR); P. parvulum sp. nov. has short (<2 cm), unbranched protuberances and attached margins and is restricted to the central and southern GBR; and P. pinnaculum sp. nov. has a mountain-like, columnar morphology and occurs on oceanic Coral Sea reefs. A rbcL gene sequence of the isotype of P. castellum demonstrates it is a different species from other columnar species. In addition to the diagnostic rbcL and psbA marker sequences, the four new species may be distinguished by a combination of features including thallus growth form, margin shape (attached or unattached), and medullary system (coaxial or plumose). Porolithon species, because of their ecological importance and sensitivity to ocean acidification, need urgent documentation of their taxonomic diversity.     

Investigating seed bank potential of crustose coralline algae using DNA metabarcoding

To examine the potential for the autogenic ecosystem engineers, crustose coralline algae (CCA), to serve as seed banks or refugia for life stages of other species, it is critical to develop sampling protocols that reflect the diversity of life present. In this pilot study on two shallow water species of CCA collected from Raoul Island (Kermadec Islands; Rangitāhua) New Zealand, we investigated two preservation methods (ethanol vs. silica gel), sampled inner and outer regions of the crusts, and used DNA metabarcoding and seven genes/gene regions (16S rRNA, 18S rRNA, 23S rRNA, cox1, rbcL, and tufA genes and the ITS rRNA region) to develop a protocol for taxa identification. The results revealed immense diversity, with typically more taxa identified within the inner layers than the outer layers. As highlighted in other metabarcoding studies and in earlier work on rhodoliths (nodose coralline algae), reference databases are incomplete, and to some extent, the use of multiple markers mitigates this issue. Specifically, the 23S rRNA and rbcL genes are currently more suitable for identifying algae, while the cox1 gene fares better at capturing the diversity present inclusive of algae. Further investigation of these autogenic ecosystem engineers that likely act as marine seed banks is needed.     

Ocean acidification weakens the structural integrity of coralline algae

The uptake of anthropogenic emission of carbon dioxide is resulting in a lowering of the carbonate saturation state and a drop in ocean pH. Understanding how marine calcifying organisms such as coralline algae may acclimatize to ocean acidification is important to understand their survival over the coming century. We present the first long‐term perturbation experiment on the cold‐water coralline algae, which are important marine calcifiers in the benthic ecosystems particularly at the higher latitudes. Lithothamnion glaciale, after three months incubation, continued to calcify even in undersaturated conditions with a significant trend towards lower growth rates with increasing pCO₂. However, the major changes in the ultra‐structure occur by 589 μatm (i.e. in saturated waters). Finite element models of the algae grown at these heightened levels show an increase in the total strain energy of nearly an order of magnitude and an uneven distribution of the stress inside the skeleton when subjected to similar loads as algae grown at ambient levels. This weakening of the structure is likely to reduce the ability of the alga to resist boring by predators and wave energy with severe consequences to the benthic community structure in the immediate future (50 years).     

TEMPERATURE CONTROLS ON CORALLINE ALGAL SKELETAL GROWTH1

Many marine and terrestrial organisms lay down regular growth bands. In some species (e.g., trees), control of growth band geometry is related to environmental conditions. Coralline algae are long‐lived marine plants with a global distribution that lay down regular calcitic growth bands composed of more‐ and less‐extensively calcified cells. Little is known about environmental and organism controls on their growth. In this investigation, coralline algae (Lithothamnion glaciale Kjellm.) were grown at 8, 11, and 15°C, and temperature controls on algal growth were considered. Calcite density within less‐extensively calcified cells in L. glaciale was negatively correlated to summer temperature. No relationships were observed between temperature and calcite density in more‐extensively calcified cells or growth‐band width itself. Additionally, temperature controls on growth in three L. glaciale thalli over the last 50 years were considered. Temperature was negatively related to calcite density in more‐ and less‐extensively calcified cells but showed no consistent relationship with band width.     

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.     

Coralline algal facies and their palaeoenvironments in the Late Eocene of Northern Italy (Calcare di Nago, Trento)

Summary The Calcare di Nago is a carbonate unit of Middle-Late Eocene (Bartonian and Priabonian) age which is well exposed at the north-eastern end of Lake Garda, on the western margin of the Lessini Shelf (Southern Alps). This unit is highly fossiliferous as far as the coralline red algae and large foraminifera are concerned. Corals, bryozoans, echinoderms, and molluscs are also present. The present study deals with the relationships among the coralline taxa, the coralline growth-forms, and their facies development in the Priabonian part of the type section of the Calcare di Nago. The taxonomic investigation led to the identification of 15 coralline red algal species belonging to 7 non-geniculate and 2 geniculate genera. One species of Peyssonneliacean (red alga) and one of Halimedacean (green alga) were also recognized. The quantitative and qualitative analyses based on coralline red algae and large foraminifera enabled five facies to be distinguished: Algal crust-branch rudstone, Algal/Discocyclina packstone, Coralalgal boundstone, Rhodolith mound wacke/packstone, and Rhodolith pavement. According to the coralline assemblages, coralline growth-forms, and large foraminiferal associations, the five facies reflect solid and soft substrate types. Some of these facies are dominated byin situ rhodoliths, others by reworked algal debris. In the architecture of an interpreted prograding carbonate ramp, shallow water facies are dominated by members of the subfamily Mastophoroideae, while deeper water facies are dominated by those of the subfamily Melobesioideae and family Sporolithaceae. There is a significant increase both in size and in constructional voids of the rhodoliths with depth. A concomitant decrease in algal species diversity with depth has been also recognized. LargeDiscocyclina assemblages are localized across the inner and mid ramp boundary.Pellatispira andBiplanispira are present only in the uppermost mid-ramp.Nummulites, Assilina, andSpiroclypeus are dominant together with small orthophragminids both in the mid- and uppermost outer ramp facies.     

Influences of salinity on the physiology and distribution of the Arctic coralline algae,Lithothamnion glaciale (Corallinales,Rhodophyta)

In Greenland, free‐living red coralline algae contribute to and dominate marine habitats along the coastline. Lithothamnion glaciale dominates coralline algae beds in many regions of the Arctic, but never in Godthåbsfjord, Greenland, where Clathromorphum sp. is dominant. To investigate environmental impacts on coralline algae distribution, calcification and primary productivity were measured in situ during summers of 2015 and 2016, and annual patterns of productivity in L. glaciale were monitored in laboratory‐based mesocosm experiments where temperature and salinity were manipulated to mimic high glacial melt. The results of field and cold‐room measurements indicate that both L. glaciale and Clathromorphum sp. had low calcification and photosynthetic rates during the Greenland summer (2015 and 2016), with maximum of 1.225 ± 0.17 or 0.002 ± 0.023 μmol CaCO ₃ · g^?1 · h^?1 and ?0.007 ±0.003 or ?0.004 ± 0.001 mg O₂ · L^?1 · h^?1 in each species respectively. Mesocosm experiments indicate L. glaciale is a seasonal responder; photosynthetic and calcification rates increase with annual light cycles. Furthermore, metabolic processes in L. glaciale were negatively influenced by low salinity; positive growth rates only occurred in marine treatments where individuals accumulated an average of 1.85 ± 1.73 mg · d^?1 of biomass through summer. These results indicate high freshwater input to the Godthåbsfjord region may drive the low abundance of L . glaciale , and could decrease species distribution as climate change increases freshwater input to the Arctic marine system via enhanced ice sheet runoff and glacier calving.     

BIODIVERSITY OF CORALLINE ALGAE IN THE NORTHEASTERN ATLANTIC INCLUDING CORALLINA CAESPITOSA SP. NOV. (CORALLINOIDEAE,RHODOPHYTA)1

The Corallinoideae (Corallinaceae) is represented in the northeastern Atlantic by Corallina officinalis L.; Corallina elongata J. Ellis et Sol.; Haliptilon squamatum (L.) H. W. Johans., L. M. Irvine et A. M. Webster; and Jania rubens (L.) J. V. Lamour. The delimitation of these geniculate coralline red algae is based primarily on morphological characters. Molecular analysis based on cox1 and 18S rRNA gene phylogenies supported the division of the Corallinoideae into the tribes Janieae and Corallineae. Within the Janieae, a sequence difference of 46–48 bp (8.6%–8.9%) between specimens of H. squamatum and J. rubens in the cox1 phylogeny leads us to conclude that they are congeneric. J. rubens var. rubens and J. rubens var. corniculata (L.) Yendo clustered together in both phylogenies, suggesting that for those genes, there was no genetic basis for the morphological variation. Within the Corallineae, it appears that in some regions, the name C. elongata has been misapplied. C. officinalis samples formed two clusters that differed by 45–54 bp (8.4%–10.0%), indicating species‐level divergence, and morphological differences were sufficient to define two species. One of these clusters was consistent with the morphology of the type specimen of C. officinalis (LINN 1293.9). The other species cluster is therefore described here as Corallina caespitosa sp. nov. This study has demonstrated that there is a clear need for a revision of the genus Corallina to determine the extent of “pseudocryptic” diversity in this group of red algae.     

Coralline algal structure is more sensitive to rate,rather than the magnitude,of ocean acidification

Marine pCO₂ enrichment via ocean acidification (OA), upwelling and release from carbon capture and storage (CCS) facilities is projected to have devastating impacts on marine biomineralisers and the services they provide. However, empirical studies using stable endpoint pCO₂ concentrations find species exhibit variable biological and geochemical responses rather than the expected negative patterns. In addition, the carbonate chemistry of many marine systems is now being observed to be more variable than previously thought. To underpin more robust projections of future OA impacts on marine biomineralisers and their role in ecosystem service provision, we investigate coralline algal responses to realistically variable scenarios of marine pCO₂ enrichment. Coralline algae are important in ecosystem function; providing habitats and nursery areas, hosting high biodiversity, stabilizing reef structures and contributing to the carbon cycle. Red coralline marine algae were exposed for 80 days to one of three pH treatments: (i) current pH (control); (ii) low pH (7.7) representing OA change; and (iii) an abrupt drop to low pH (7.7) representing the higher rates of pH change observed at natural vent systems, in areas of upwelling and during CCS releases. We demonstrate that red coralline algae respond differently to the rate and the magnitude of pH change induced by pCO₂ enrichment. At low pH, coralline algae survived by increasing their calcification rates. However, when the change to low pH occurred at a fast rate we detected, using Raman spectroscopy, weaknesses in the calcite skeleton, with evidence of dissolution and molecular positional disorder. This suggests that, while coralline algae will continue to calcify, they may be structurally weakened, putting at risk the ecosystem services they provide. Notwithstanding evolutionary adaptation, the ability of coralline algae to cope with OA may thus be determined primarily by the rate, rather than magnitude, at which pCO₂ enrichment occurs.     

Natural inducers for coral larval metamorphosis

 Coral gametes from Acropora millepora (Ehrenberg, 1834) and from multi-species spawning slicks provided larvae for use in metamorphosis assays with a selection of naturally occurring inducer chemicals. Four species of crustose coralline algae, one non-coralline crustose alga and two branching coralline algae induced larval metamorphosis. However, one additional species of branching coralline algae did not produce a larval response. Metamorphosis was also observed when larvae were exposed to skeleton from the massive coral Goniastrea retiformis (Lamarck, 1816) and to calcified reef rubble, demonstrating metamorphosis is possible in the absence of encrusting algae. Chemical extracts from these algae and the coral skeleton, obtained using either decalcification or simple methanol extraction procedures, also contained active inducers. These results extend the number of crustose algal species known to induce coral metamorphosis, suggest that some inducers may not necessarily be strongly associated with the calcified algal cell walls, and indicate that inducer sources in reef habitats may be more diverse than previously reported. Accepted: 21 May 1999