Fine structure of deep-layer sloughing and epithallial regeneration in Lithophyllum neoatalayense (Corallinales, Rhodophyta)

Transmission electron microscopic study of Lithophyllum neoatalayense Masaki demonstrated that this alga used two mechanisms by which it sloughed cells from its surface. Epithallial filaments, produced by a layer of underlying initial cells, were two to four cells long. Terminal epithallial cells, those closest to the thallus surface, underwent senescence and shedding as previously described for other coralline algae. In addition, deep-layer sloughing occurred. During this process, which is known for only one other coralline alga, cell death occurred uniformly within a surface layer 40-50 μm thick. No pathogens or evidence of mechanical damage was detected. The zone of dead cells included the epithallial layer, the layer of initial cells, and some cortex cells beneath the initials. Pit plugs connecting living and dead cells at the edge of the necrotic zone were sealed by wall material deposited by the surviving cells, but cells within the necrotic zone showed no evidence of sealed pit plugs. The outermost surviving cells became new initial cells, which then divided to form new epithallial cells. Regeneration of the epithallial layer occurred before the thick layer of dead cells peeled away. The extensive deep shedding of both epithallial and initial cells in L. neoatalayense and the effectiveness of regeneration from cortex cells challenge the assumption that protection of initial cells is an important function of epithallial cells.     

Geographic variation in the damselfish-red alga cultivation mutualism in the Indo-West Pacific

Background  

On coral reefs, damselfish defend their territories from invading herbivores and maintain algal turfs, from which they harvest filamentous algae. In southern Japan, intensive weeding of indigestible algae by Stegastes nigricans results in overgrowth by one filamentous alga, Polysiphonia sp. 1. Because this alga is highly susceptible to grazing and is competitively inferior to other algae, it survives only within the protective territories of this fish species, suggesting an obligate mutualism between damselfish and their cultivated alga. The wide distribution of damselfish species through the Indo-Central Pacific raises the question of whether this species-specific mutualism is maintained throughout the geographic range of the fish. To address this question, from all 18 damselfish species we conducted comprehensive surveys of algal flora within their territories throughout the Indo-West Pacific, and identified species of Polysiphonia using morphological examination and gene sequencing data.     

The Role of Encrusting Coralline Algae in the Diets of Selected Intertidal Herbivores

Kalk Bay, South Africa, has a typical south coast zonation pattern with a band of seaweed dominating the mid-eulittoral and between two molluscan-herbivore dominated upper and lower eulittoral zones. Encrusting coralline algae were very obvious features of these zones. The most abundant herbivores in the upper eulittoral were the limpet, Cymbula oculus (10.4 ± 1.6 individuals m⁻²; 201.65 ± 32.68 g.m⁻²) and the false limpet, Siphonaria capensis (97.07± 19.92 individuals m⁻²; 77.93 16.02 g.m⁻²). The territorial gardening limpet, Scutellastra cochlear, dominated the lower eulittoral zone, achieving very high densities (545.27 ± 84.35 m⁻²) and biomass (4630.17 ± 556.13 g.m⁻²), and excluded all other herbivores and most seaweeds, except for its garden alga and the encrusting coralline alga, Spongites yendoi (35.93 ± 2.26% cover). In the upper eulittoral zone, encrusting coralline algae were only present in the guts of the chiton Acanthochiton garnoti (30.5 ± 1.33%) and the limpet C. oculus (2.9 ± 0.34%). The lower eulittoral zone limpet, Scutellastra cochlear also had a large percentage of encrusting coralline algae in its gut with limpets lacking gardens having higher (45.1 ± 1.68%) proportions of coralline algae in their guts than those with gardens (25.6 ± 0.8%). Encrusting coralline algae had high organic contents, similar to those of other encrusting and turf-forming algae, but higher organic contents than foliose algae. Radula structure, grazing frequencies as a percentage of the area grazed (upper eulittoral 73.25 ± 3.60% d⁻¹; lower eulittoral 46.0 ± 3.29% d⁻¹), and algal organic content provided evidence to support the dietary habits of the above herbivores. The data show that many intertidal molluscs are actively consuming encrusting coralline algae and that these seaweeds should be seen as an important food source.     

Succession and growth rates of encrusting crustose coralline algae (Rhodophyta,Cryptonemiales) in the upper fore-reef environment off Ishigaki Island,Ryukyu Islands

Observations were made on the succession and growth rates of crustose coralline algae growing in situ on artificial substrata in a shallow fore-reef environment on Ishigaki Island, Ryukyu Islands. Succession in well-illuminated environments manifests itself as a gradual replacement of species having very thin thalli by those having larger and thicker thalli. The species Porolithon onkodes, Paragoniolithon conicum and Lithophyllum insipidum achieved dominance by competitive interactions of overgrowing margins. The thicker species recruit quickly (within the first few months), but because of their slow growth rate do not displace the pioneer species that have very thin thalli until after the latter begin to die. Regardless of seasonal temperature fluctuations, which exceed 10 °C, the coralline algal succession is the same for each season. The maximum lateral growth rates of the major species range between 2.9 and 3.9 mm/month. Vertical growth rates of Porolithon onkodes, the thickest species, are the most rapid (more than 2 mm/year at maximum) relative to those of other species. Accretion rates of entire coralline algal cover on ungrazed substrata range from 1.0 to 1.2 mm/year (not allowing any lag time for recruitment), whereas those of grazed substrata are lower. These results are consistent with species which are ecological equivalents and live in similar environments on Caribbean reefs.     

Facultative mutualism between an herbivorous crab and a coralline alga: advantages of eating noxious seaweeds

Because encrusting coralline algae rely on herbivory or low light levels to prevent being overgrown by competitively superior fleshy algae, corallines are relatively rare in shallow areas with low rates of herbivory. In contrast to this general trend, the branching coralline alga Neogoniolithon strictum occurs primarily in shallow seagrass beds and along the margins of shallow reef flats where herbivory on macrophytes is low. This alga apparently persists in these habitats by providing refuge to the herbivorous crab Mithrax sculptus at mean densities of 1 crab per 75 g of algal wet mass. When crabs were removed from some host corallines, hosts without crabs supported 9 times the epiphytic growth of hosts with crabs after only 30 days. Crabs without access to a coralline alga were rapidly consumed by reef fishes, while most of those tethered near a host alga survived. These results suggest that the crabs clean their algal host of fouling seaweeds and associate with the host to minimize predation. However, to effectively clean the host, the crab must consume the wide array of macroalgae that commonly co-occur with coralline algae in these habitats, including chemically defended species in the genera Halimeda, Dictyota, and Laurencia. Crabs did readily consume these seaweeds, which were avoided by, and are chemically defended from, herbivorous fishes. Even though crabs readily consumed both Halimeda and Dictyota in whole-plant feeding assays, chemical extracts from these species significantly reduced crab feeding, suggesting that factors other than secondary chemistry (e.g., food value, protein, energy content), may determine whole-plant palatability. Having the ability to use a wide variety of foods, and choosing the most profitable rather than the least defended foods, would diminish foraging time, increase site fidelity, and allow the crab to function mutualistically with the host alga. Despite the obvious benefit of associating with N. strictum, M. sculptus did not prefer it over other habitats offering a structurally similar refuge, suggesting that these crabs are not N. strictum specialists, but rather occupy multiple habitats that provide protection from predators. Structurally complex organisms like N. strictum may commonly suppress competitors by harboring protective symbionts like M. sculptus. It is possible that diffuse coevolution has occurred between these two groups; however, this seems unlikely because both herbivore and host appear to respond most strongly to selective pressures from predators and competitors outside this association.     

THE SIGNIFICANCE OF REPRODUCTIVE AND SPORE GERMINATION CHARACTERISTICS TO THE SYSTEMATIC OF THE CORALLINACEAE: NONARTICULATED CORALLINE ALGAE12

This paper deals with reproductive and spore germination characteristics to the systematics of the nonarticulated coralline algae. As can the articulated coralline algae, the nonarticulated coralline algae may also he divided into 2 groups on the basis of their yearly reproductive cycles, spore dimensions, and spore germination characteristics: the Lithophyllum group and the Lithothamnium group. These 2 groups are basically identical with the Amphiroa and Corallina groups of the articulated coralline algae, respectively, so far as these 3 characters are concerned. The grouping of these representatives of the Corallinaceae into 2 groups—Amphiroa—Lithophyllum and Corallina–Lithothamnium—coincides with a grouping based on the manner of connection between cells of adjacent filaments.     

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     

THE MORPHOLOGY OF CUBICULOSPORUM KORONICARPIS GEN. ET SP. NOV., REPRESENTING A NEW FAMILY IN THE GIGARTINALES (RHODOPHYTA)

The red alga Cubiculosporum koronicarpis gen. et sp. nov. is described from material collected during 1968 in the Philippines. The species differs substantially in regard to its carposporophyte development from other red algae in the order Gigartinales, and a new family is created based on its unique combination of reproductive features. A single, short, connecting filament is formed between the fertilized carpogonium and a nearby auxiliary cell. The latter produces several ramifying gonimoblast filaments towards the interior of the thallus. No fusion cell is formed and the gonimoblast filaments grow inward among the cells of the central axis, form secondary connections to them, and give rise to outwardly directed carposporangial filaments that develop within peripheral chambers formed between elongating inner cortical cells. The alga is a low, clump-forming species of well-washed intertidal reef platforms at the one Philippine locality where it has been found. There it contributed a uniform but very minor amount to the wet weight of the standing crops that were studied during two separate seasons of the year.     

Lithophyllum cuneatum sp. nov. (Corallinaceae, Rhodophyta), a new species of non-geniculate coralline alga semi-endophytic in Hydrolithon onkodes and Neogoniolithon sp. from Fiji, South Pacific

A new species of semi-endophytic coralline alga, Lithophyllum cuneatum (Corallinaceae: Lithophylloideae), is described from Fiji. The species is characterized by a wedge-like thallus that is partially buried in the thallus of the host coralline, Hydrolithon onkodes (Heydrich) Penrose et Woelkerling or occasionally Neogoniolithon sp., and that appears at the surface of the host as a small pustule that is usually paler in color than the host. The thallus consists of erect filaments that are derived from a single cell. The basal cell, when visible, is non-palisade, and areas of bistratose margin are absent. Cells of contiguous erect filaments are joined by secondary pit connections. Epithallial cells are present in 2–3 layers, and individual trichocytes are common. Gametangial plants are dioecious. Male conceptacles have simple spermatangial systems that are confined to the floors of their elliptical chambers. Carposporangial conceptacles contain 5–8 celled gonimoblast filaments that are borne at the margin of a more-or-less discoid fusion cell, and so occupy the periphery of the elliptical conceptacle chambers. Tetrasporangial conceptacles are uniporate, with roofs formed from peripheral filaments, and chambers lack a central columella of sterile filaments. Despite its semi-endophytic nature, haustorial cells are absent, and plastids and pigmentation are present.     

Relationship between cover of Chondrus crispus (Gigartinales,Rhodophyta) and Phymatolithon (Corallinales,Rhodophyta) on friable rock substrata

Field observations in sublittoral Prince Edward Island, Canada, indicated that on a friable sandstone substratum Chondrus crispus was more commonly associated with Phymatolithon sp. than with bare rock. Thus, a substantial proportion of the population of Irish moss along the coast of Prince Edward Island occurs on this encrusting coralline. These observation may be explained on the basis of the relative stability of the substratum in contrast to other studies in which sloughing of epithallial cells by species of both Phymatolithon and Lithothamnium has been reported to limit epiphytism by fleshy macrophytes.Issued as NRCC 31426.     

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.     

SMITHSONIELLA GEN. NOV., A POSSIBLE EVOLUTIONARY LINK BETWEEN THE MULTICELLULAR AND SIPHONOUS HABITS IN THE ULVOPHYCEAE,CHLOROPHYTA

A low relief, green turf-forming alga of a heterotrichous habit was discovered in the coral reef microcosm, Museum of Natural History, Smithsonian Institution. Erect filaments bore lateral, specialized sporangia and together with basal filaments possessed septal plugs between adjacent cells, grossly similar to the “pit connections” of red algae. Data are presented which: 1) establish the identity of our plant with a plant recently described as Pilinia earleae Gallagher et Humm from the Florida Gulf coast; 2) support our establishment of the new genus Smithsoniella and our transfer of P. earleae to this new taxon. Additional data on pigmentation and cytology are related to the fine structure of other selected green algae to develop and test three hypotheses, viz. Smithsoniella earleae represents either: 1) a symbiotic association between a green and a red alga; 2) an alga which belongs to either the Ulotrichales, Chaetophorales or the Chroolepidales; or 3) an alga representing an evolutionary link between filamentous forms of the Ulvophyceae and members of the coenocytic siphonalean complex (e.g., Codiales or Caulerpales) of the Chlorophyta. Data refute hypotheses 1 and 2 but do lend support to the third hypothesis.     

Taxonomic study of a new green alga,Annulotesta cochlephila gen. et sp. nov. (Kornmanniaceae,Ulvales, Ulvophyceae), growing on the shells of door snails

Some algae are known to grow on shellfish shells. Most of these have been reported in aquatic environments. The species specificity for substrate shells varies, and some algae grow only on the shells of a certain species of shellfish, such as Pseudocladophora conchopheria (Cladophorales, Ulvophyceae) on Lunella coreensis (Trochida, Gastropoda). There are very few reports of algae that grow on land snails. In this study, we discovered green algae growing on the shells of six species of door snails (Clausiliidae) from nine localities in Japan. These green algae formed a green mat composed of thalli embedded in the extracellular matrix. The thallus was composed of aggregated oval cells and peripheral branched filaments. The cells possessed a single parietal chloroplast with a pyrenoid surrounded by two starch sheaths and transversed by a thylakoid. Oil droplets in the cell and ring-like structures on the cell wall surface were frequently observed. The 18S rDNA sequences of all shell-attached algae on different clausiliid species from different localities were almost identical and formed a new clade in the family Kornmanniaceae (Ulvales, Ulvophyceae). No other algae forming visible colonies on the clausiliid shell were found. These findings indicate the presence of specificity between the alga and clausiliid shells. Based on the results of morphological observation and molecular phylogenetic analysis, we propose a new genus and new species of shell-attached green alga, Annulotesta cochlephila.

     

PRODUCTS OF PHOTOSYNTHESIS IN CAULERPA SIMPLICIUSCULA (CHLOROPHYCEAE)1

The kinetics of carbon flow through various metabolites of Caulerpa simpliciuscula C. Ag., a siphonaceous green alga, are described. The pattern of C fixation in this alga differs from those observed in higher plants and other green algae in a number of respects. After 40 min incubation, soluble β-linked polyglucans are the most important labelled carbohydrates. Sucrose, although delectable, is never a major recipient of label and does not label until after other oligosaccharide fractions. The sugar monophosphates contain a large proportion of the ¹⁴C assimilated even after 40 min and behave not only as metabolic intermediates, but also as storage pools. The pattern of ammo acid labelling resembles that reported for other species of green algae in that alanine becomes labelled most rapidly, followed by glycine, and much later by glutamate, glutamine and asparagine. These labelling patterns are discussed in the light, of what is known of patterns of C flow in other algae.     

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.     

THE OCCURRENCE,EVOLUTION, AND PHYLOGENETIC SIGNIFICANCE OF PARENCHYMA IN COLEOCHAETE BRÉB. (CHLOROPHYTA)

Thalli of four species of the charophycean green alga Coleochaete Bréb.; C. irregularis, C. soluta, C. orbicularis, and C. scutata, were examined using light and electron microscopy. The parenchymatous nature of the plant bodies of C. orbicularis and C. scutata became apparent when the degree of cellular association in these species was compared with that of parenchymatous land plant tissues, the pseudoparenchymatous thalli of C. soluta, and the branched filaments of C. irregularis. Coleochaete soluta was shown to be morphologically and phylogenetically transitional between the more primitive branched filamentous species (C. irregularis) and the more advanced discoid species (C. orbicularis and C. scutata). The branching patterns observed in C. soluta suggested a possible pathway for the evolutionary development of land plant parenchyma from branched, filamentous charophycean green algae.     

Consistency in a marine algal‐grazer interaction over multiple scales

Coralline algae are conspicuous members of many marine assemblages, especially those characterized by intense grazing pressure. We explored whether articulated species, especially Corallina vancouveriensis, depend on grazing invertebrates to both establish and flourish in an exposed rocky intertidal setting, and whether this plant–grazer relationship varied over more than three orders of magnitude (≈100–>300,000 μm). Three experimental manipulations, supplemented by observations on recruitment, demonstrated that (i) C. vancouveriensis failed to recover rapidly from disturbed areas when grazers were experimentally excluded; (ii) recruitment occurred in the presence of grazers; (iii) increasing surface texture of molded surfaces enhanced coralline recruitment more when grazers were present; and (iv) settlement occurred predominately in microtopographical low areas of a molded surface, whereas a competitively superior fleshy red alga tended to recruit to high areas. These results confirm that coralline algal establishment and persistence are enhanced by grazers and reveal that this relationship is consistent over a range of biologically relevant scales.     

Crustose coralline algae and associated microbial biofilms deter seaweed settlement on coral reefs

Crustose coralline algae (CCA), a group of calcifying red algae found commonly in benthic marine ecosystems worldwide, perform essential ecological functions on coral reefs, including creating benthic substrate, stabilizing the reef structure and inducing coral settlement. An important feature of CCA is the ability to keep their surfaces free of epiphytic algae, thereby reducing algal overgrowth and allowing them access to light. However, the mechanisms by which CCA prevent settlement of opportunistic seaweeds (fleshy macroalgae) are not fully understood, nor is whether these mechanisms vary among CCA species. In our study based on the Great Barrier Reef, we demonstrate that three common CCA species (Titanoderma pustulatum, Porolithon onkodes and Neogoniolithon sp.) have a remarkable ability to deter settlement of seaweed spores. We provide experimental evidence that the CCA use allelopathy and microbial inhibition against the settlement of spores of the brown seaweed Padina boergesenii. Methanol extracts of allelopathic compounds from T. pustulatum, Po. onkodes and Neogoniolithon sp. significantly reduced the settlement of Pa. boergesenii spores by 4.3 times, 3.0 and 3.8 times, respectively. Further, we found that microbial biofilms, while having a lower inhibitory effect than allelopathic compounds, also reduced seaweed settlement of Pa. boergesenii. Our study demonstrates that allelopathy and microbial inhibition, in addition to epithallial tissue sloughing, are mechanisms employed by CCA to prevent the settlement of epiphytic algae. Understanding the mechanisms by which CCA avoid seaweed overgrowth contributes to our understanding of the dynamics of seaweed proliferations on reefs and to the ecological knowledge of this important group of reef-building organisms.     

INTERACTIONS BETWEEN OCEAN ACIDIFICATION AND WARMING ON THE MORTALITY AND DISSOLUTION OF CORALLINE ALGAE1

Coralline algae are among the most sensitive calcifying organisms to ocean acidification as a result of increased atmospheric carbon dioxide (pCO₂). Little is known, however, about the combined impacts of increased pCO₂, ocean acidification, and sea surface temperature on tissue mortality and skeletal dissolution of coralline algae. To address this issue, we conducted factorial manipulative experiments of elevated CO₂ and temperature and examined the consequences on tissue survival and skeletal dissolution of the crustose coralline alga (CCA) Porolithon (=Hydrolithon) onkodes (Heydr.) Foslie (Corallinaceae, Rhodophyta) on the southern Great Barrier Reef (GBR), Australia. We observed that warming amplified the negative effects of high pCO₂ on the health of the algae: rates of advanced partial mortality of CCA increased from <1% to 9% under high CO₂ (from 400 to 1,100 ppm) and exacerbated to 15% under warming conditions (from 26°C to 29°C). Furthermore, the effect of pCO₂ on skeletal dissolution strongly depended on temperature. Dissolution of P. onkodes only occurred in the high‐pCO₂ treatment and was greater in the warm treatment. Enhanced skeletal dissolution was also associated with a significant increase in the abundance of endolithic algae. Our results demonstrate that P. onkodes is particularly sensitive to ocean acidification under warm conditions, suggesting that previous experiments focused on ocean acidification alone have underestimated the impact of future conditions on coralline algae. Given the central role that coralline algae play within coral reefs, these conclusions have serious ramifications for the integrity of coral‐reef ecosystems.