Experimental effects of kelp canopies on subtidal coralline algae

Plants are often grouped as canopy species or understorey species because it is thought that that these sets of taxa interact in predictable ways. Mensurative experiments in southern Australia demonstrated that the percentage cover of encrusting coralline algae was greater, and articulated (branching) coralline algae less, on boulders under a canopy of dense kelp (>7 plants per m²), Ecklonia radiata, than on boulders without kelp. Experimental clearances of kelp and reciprocal transplants of boulders between patches of E. radiata and patches without kelp showed that canopies maintained and facilitated the growth of encrusting coralline algae and reduced the cover of articulated coralline algae. Potential artefacts associated with clearing kelp and transplanting boulders were not detected when tested with a series of translocation controls. These results reject the model that the co‐occurrence of E. radiata and encrusting corallines is just an assemblage of plants caused by spatial and temporal coincidence. Instead, they support the model that kelp facilitates the growth and survival of understorey algae.     

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.     

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.     

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.     

LITOSTROMA,A NEW GENUS OF PROBLEMATICAL ALGAE FROM THE PENNSYLVANIAN OF OKLAHOMA

Mamay , Sergius H. (U. S. Geological Survey, Washington, D. C.) Litostroma, a new genus of problematical algae from the Pennsylvanian of Oklahoma. Amer. Jour. Bot. 46(4): 283–292. Illus. 1959.—Litostroma oklahomense, gen. et sp. nov. is described on the basis of fossil plant material found in a Pennsylvanian marine limestone from the vicinity of McAlester, Oklahoma. Litostroma is a simple plant consisting of a small, irregularly shaped thallus 1 cell thick. Some thalli have small perforations and filament-like marginal outgrowths. The reproductive organs are not known. A marine fauna is intimately associated with Litostroma, and includes epiphytic Foraminifera preserved in actual growth positions on surfaces of the plants. The evidence indicates a marine habitat for Litostroma and, accordingly, algal affinity. Without information bearing on its reproductive organs or pigmentation, however, Litostroma cannot with assurance be assigned to any known group of algae. It possibly represents a group of green, brown, or even red algae.     

The bacterial biota on crustose (nonarticulated) coralline algae from Tasmanian waters

The bacterial biota associated with the cuticle surface of healthy benthic samples of crustose nonarticulated coralline algae from the east coast of Tasmania (Australia) was examined by bacteriological cultivation and electron microscopy. In 32 samples studied, the viable count on Zobell's marine agar (supplemented with vitamins) was 3.3×10⁶ bacteria g^–1 wet wt. (range 2.9×10⁴–2.7×10⁷). Of 732 strains isolated from 16 out of 32 samples and identified to genus level,Moraxella was the predominant genus (66%). In contrast,Moraxella comprised only 11% of 217 strains isolated from benthic seawater samples collected at the same time as coralline algae. In 22 out of 32 algal samples examined by scanning electron microscopy, the total count was 1.6 × 10⁷ bacteria g^–1 wet wt. (range 5.1× 10⁶–3.8×107); the major morphotype was cocco-bacilli (80%). Several environmental factors did not significantly influence the viable count or generic distribution, or the total count or morphotypic distribution of bacteria on the cuticle. These factors included geographical site, season, storage of samples in aquarium conditions, and the presence or absence of abalone from shells that the coralline algae encrusted. The microbiota, consisting mostly of the nonmotile bacterial genusMoraxella, appeared to be highly adapted to its calcerous plant host.     

Predicting understorey structure from the presence and composition of canopies: an assembly rule for marine algae

Assembly rules provide a useful framework for predicting patterns of community assembly under defined environmental conditions. Habitat created by canopy-forming algae (such as kelps) provides a promising system for identifying assembly rules because canopies typically have a large and predictable influence on understorey communities. Across >1,000 km of subtidal South Australian coastline, we identified natural associations between assemblages of understorey algae and (1) monospecific canopies of Ecklonia radiata, (2) canopies comprised of E. radiata mixed with Fucales (Cystophora spp. and Sargassum spp.), and (3) gaps among canopies of algae. We were able to recreate these associations with experimental tests that quantified the assembly of understorey algae among these three habitat types. We propose the assembly rule that understorey communities on subtidal rocky coast in South Australia will be (1) monopolised by encrusting coralline algae beneath monospecific canopies of E. radiata, (2) comprised of encrusting corallines, encrusting non-corallines, and sparse covers of articulated corallines, beneath mixed E. radiata-Fucales canopies, and (3) comprised of extensive covers of articulated corallines and filamentous turfs, as well as sparse covers of foliose algae and juvenile canopy-formers, within gaps. Consistencies between natural patterns and experimental effects demonstrate how algal canopies can act as a filter to limit the subsets of species from the locally available pool that are able to assemble beneath them. Moreover, the subsets of species that assemble to subtidal rocky substrata in South Australia appear to be predictable, given knowledge of the presence and composition of canopies incorporating E. radiata.     

The larval and juvenile ecology of the temperate octocoral Alcyonium siderium Verrill. I. Substratum selection by benthic Larvae

The Alcyonacean octocoral Alcyonium siderium Verrill forms dense stands on vertical rock walls (6–18 m subtidal) along the coast of Massachusetts and further north into the Gulf of Maine. Larvae are brooded until their release as crawling demersal planulae in August. Each colony produces several hundred larvae; most crawl onto the nearby substratum although others may be carried away by wave surge.Experimental enclosures were used to examine substratum selection in the field. Planulae metamorphosed in greater numbers than expected by percent cover on the fleshy red crustose alga Waernia mirabilis Wilce (proposed). The crustose coralline algae Phymatolithon rugulosum (Foslie) and Lithothamnium glaciale Kjellman were settled on commonly but less often than expected by their percent cover. Bare rock surfaces were also used, but least frequently. The encrusting invertebrate colonies that cover much of the available substratum were never used as sites of settlement and metamorphosis. These results agree with laboratory evidence that settlement and metamorphosis of Alcyonium planulae can be induced by Waernia and by coralline algae.     

RADIOISOTOPIC STUDY OF CALCIFICATION IN THE ARTICULATED CORALLINE ALCA BOSSIELLA ORBIGNIANA1

Calcification in Bossiella orbigniana (Corallinaceae) is characterized by a series of features which, vary according to the age of the segment (intergeniculum). From the youngest segment at the branch tip to older, more basal segments: (1) weight and degree of mineralization increase, while rate of weight gain decreases; (2) rate and stability of calcium-45 labeling decrease; (3) effect of light on calcium-45 labeling rate decreases, while effect of light on stability of label increases; however, for all segments, calcium-45 labeling is more rapid and more stable in the light than in the dark; (4) rate of calcium-45 labeling in killed controls decreases. Comparative studies with the tropical coralline alga Amphiroa yielded similar results. Characteristics of the gradients in calcification and effect of light in these coralline algae are very similar to those found, in a reef-building coral containing symbiotic algae, and the data suggest that organic products of photosynthesis may be of general importance to calcification.     

TYPES OF LATICIFERS AND CRYSTALS IN JATROPHA AND THEIR TAXONOMIC IMPLICATIONS

Anatomical examination of 37 species of Jatropha (Euphorbiaceae) has revealed the occurrence of two distinct types of laticifers—articulated, and nonarticulated—in addition to idioblasts that are irregularly shaped individual cells. With the notable exception of J. augustii Pax & K. Hoffm. (section Peltatae (Pax) Dehgan & Webster), these idioblasts occur in the two most advanced sections of the subgenus Curcas (Adans.) Pax, namely Loureira (Cav.) Muell. Arg. ex Pax and Mozinna (Ortega) Pax. The presence of two laticifer types and “idioblastic laticifers” in the genus, in association with the morphological reduction series found with evolutionary advancement are, therefore, significant in the delimitation of sections and subsections. Further evidence is presented by the occurrence of “chambered crystalliferous cells” in subgenus Curcas, but not in subgenus Jatropha (=Adenorhopium Griseb.). Reexamination of laticifers in other genera of the Euphorbiaceae is suggested as a possible means of alleviating the long-standing taxonomic dilemma of this large and morphologically diverse family.     

ZONATION OF DEEP WATER BENTHIC ALGAE IN THE GULF OF MAINE1

Algal community structure is described for a deep-water rock pinnacle in the Gulf of Maine. Three depth zones of algal dominance were apparent consisting of 1) leathery macrophytes (to 40 m), 2) foliose red algae (to 50 m) and 3) crustose algae (fleshy crusts to 55 m and coralline crusts to 63 m). Microscopic filamentous and erect calcareous algae were also present but inconspicuous. Upright macroscopic filamentous and thin sheet-like forms were not observed on the pinnacle. Sea anemones (Metridium senile) dominated some vertical faces and abrupt prominences in the shallowest regions of the pinnacle (to 24 m) and locally appeared to set the upper vertical limits of kelp and possibly foliose reds. Laminaria sp. formed an open park-like canopy from 24 to 30 m whereas Agarum cribrosum, the deepest kelp, grew as isolated individuals to 40 m. Peyssonnelia sp. and Leptophytum laeve were the deepest occurring fleshy (to 55 m) and calcareous crusts (to 63 m), respectively. The occurrence of these algae at record depths for the Gulf of Maine and for cold water marine environments may be the result of an absence of large herbivores and the high productivity potential of the benthos in these relatively clear waters. By compiling data on depth distribution patterns world-wide, it is evident that the three zone structure of algal morphologies observed in the Gulf of Maine is a global phenomenon.     

THE SPORE-GERMINATION PATTERN OF THELYPTEROID FERNS

Cell division patterns in germinating spores of several Thelypteris species were studied using light microscopy of sectioned material and scanning electron microscopy. All species exhibited the same basic germination pattern, characterized by an asymmetric cell division of the spore parallel to the equatorial plane to delimit a proximal rhizoid, followed by a perpendicular division of the basal cell to form the protonemal cell. While spore-germination patterns appear to be a potentially useful taxonomic character in some groups of ferns, the homogeneity in this character exhibited by the thelypteroid group impairs its usefulness in the taxonomy of Thelypteris.     

THE EFFECT OF TEMPERATURE AND PHOTOPERIOD ON THE DEVELOPMENT OF GEOGRAPHICALLY ISOLATED POPULATIONS OF FUNARIA HYGROMETRICA AND WEISSIA CONTROVERSA

Geographically isolated populations of Funaria hygrometrica Hedw. and Weissia controversa Hedw. were cultured under controlled axenic conditions in the laboratory to determine the developmental variability found between and within two species of widespread distribution. Funaria plants were found to grow more rapidly than those of Weissia; the latter could not be induced to complete the life cycle in culture, and generally had a less broad tolerance to environmental extremes than did Funaria. Optimum temperatures of 30 C for spore germination and 25 C for protonematal growth and gametophore formation were observed in all populations of Funaria. Gametangial formation required cooler temperatures in all populations; however, optimal temperature requirements and sporophytic growth characteristics were population-dependent. The temperature responses of the various stages of the life cycle correlate well with seasonal temperature fluctuations that might be expected in nature. The presence of ecological races in Funaria hygrometrica is demonstrated in the behavior of the reproductive stages of the life cycle.     

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.     

Multiple allelopathic activity of the crustose coralline algaLithophyllum yessoenseagainst settlement and germination of seaweed spores

A study was made to investigate possible formation by the crustose coralline algaLithophyllum yessoenseof multiple allelopathic-related substances against the settlement and germination of spores of various seaweeds. Seven different solvents (n-hexane, diethyl ether, acetone, ethyl acetate, acetonitrile, methanol, distilled water) and seawater were used to obtain crude extracts and secretory exudates from the coralline alga. The extracts and the algal conditioned seawater were tested for inhibitory activity against the settlement and germination of spores from 17 species representing 15 genera. Spore settlement of 14 species was inhibited over 90% by one or more extracts of the six organic solvents and conditioned seawater. The germination of spores from 13 species was inhibited by one or more extracts of all seven solvents and conditioned seawater. The species where spore settlement was not significantly affected showed strong inhibition of germination, andvice versa.     

COMPARATIVE DEVELOPMENT OF THE RED ALGAL PARASITES BOSTRYCHIOCOLAX AUSTRALIS GEN. ET SP. NOV. AND DAWSONIOCOLAX BOSTRYCHIAE (CHOREOCOLACACEAE,RHODOPHYTA)1

The development of two red algal parasites was examined in laboratory culture. The red algal parasite Bostrychiocolax australis gen. et sp. nov., from Australia, originally misidentified as Dawsoniocolax bostrychiae (Joly et Yamaguishi-Tomita) Joly et Yamaguishi-Tomita, completes its life history in 6 weeks on its host Bostrychia radicans (Montagne) Montagne. Initially the spores divide to form a small lenticular cell, and then a germ tube grows from the opposite pole. Upon contact with the host cuticle, the germ tube penetrates the host cell wall. The tip of the germ tube expands, and the spore cytoplasm moves into this expanded tip. The expanded germ tube tip becomes the first endophytic cell from which a parasite cell is cut off that fuses with a host tier cell. The nuclei of this infected host cell enlarge. As parasite development continues, other host-parasite cell fusions are formed, transferring more parasite nuclei into host cells. The erumpent colorless multicellular parasite develops externally on the host, and reproductive structures are visible within 2 weeks. Tetrasporangia are superficial and cruciately or tetra-hedrally divided. Spermatia are formed in clusters. The carpogonial branches are four-celled, and the carpogonium fuses directly with the auxiliary (support) cell. The mature carposporophyte has a large central fusion cell and sympodially branched gonimoblast filaments. Early stages of development differ markedly in Dawsoniocolax bostrychiae from Brazil. Upon contact with the host, the spore undergoes a nearly equal division, and a germ tube elongates from the more basal of the two spore cells, penetrates the host cell wall, and fuses with a host tier cell. Subsequent development involves enlargement of the original spore body and division to form a multicellular cushion, from which descending rhizoidal filaments form that fuse with underlying host cells. This radically different development is in marked contrast to the final reproductive morphology, which is similar to B. australis and has lead to taxonomic confusion between these two entities. The different spore germination patterns and early germ-ling development of B. australis and D. bostrychiae warrant the formation of a new genus for the Australian parasite.     

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.     

SPORE GERMINATION AND EARLY DEVELOPMENT OF THE GAMETOPHYTE OF SCHIZAEA PUSILLA

During germination of the spore of Schizaea pusilla, the first division of the protoplast was perpendicular to the polar axis and resulted in the formation of the rhizoid. The next division parallel to the polar axis of the spore gave rise to the protonemal initial. Following this “Vittaria”-type germination, the protonema that developed was characterized by an extensive branching to produce uniseriate filaments and rhizoidophores.     

THE ULTRASTRUCTURE OF MEIOSPORES OF COLEOCHAETE PULVINATA (CHAROPHYCEAE)1

In view of the relative importance of reproductive cell ultrastructure in phylogenetic and systematic studies of green algae, we investigated the fine structure of germinating zygotes and meiospores of Coleochaete pulvinata Braun. Meiospores have a flagellar apparatus very similar to that of zoospores and spermatozoids of the same species. Meiospores differ from zoospores and spermatozoids of C. pulvinata in having pyramidal body scales similar to those present on zoospores of C. scutata. Meiospores of C. pulvinata had as many as twice the number of spline microtubules as zoospores, and four times the number present in splines of spermatozoids of the same species. Developing meiospores of C.pulvinata, like those of other Coleochaete species, are individually surrounded by chamber walls. These differed from vegetative cell walls in lacking plasmodesmata. Moreover, the chamber walls in germinating zygotes of C.pulvinata stained a cobalt blue color with resorcinal blue, and fluoresced yellow in the presence of aniline blue, thus exhibiting the staining characteristics of callose. In location, morphology and presence of callose, chamberwalls resemble “special walls” of land plants, they may represent a charophycean spore development preadaptation useful in the evolution of walled spores characteristic of land