FACTORS AFFECTING THE RATE OF CALCIFICATION IN HALIMEDA OPUNTIA (L.) LAMOUROUX AND HALIMEDA DISCOIDEA DECAISNE1

Halimeda is a prominent part of the calcifying algae in the coral-reef lagoon ecosystems in the Caribbean. Experiments were performed on the Cayo Enrique Reef off Puerto Rico and in the laboratories of the University of Maryland to study factors influencing the calcification processes. Halimeda opuntia has a higher percentage of calcium carbonate than does Halimeda discoidea and a faster rate of incorporation. Halimeda opuntia and Halimeda discoidea show a stimulation of incorporation by light as well as a diurnal rhythm under identical conditions of illumination. Both phenomena parallel the rhythm of chloroplast migration within the plant. Calcification is also stimulated by the addition of carbon dioxide. Such evidence clearly indicated a light-linked mechanism which could involve photo-synthesis. However other metabolic processes, such as respiration, are also implicated. Aeration alone accelerates calcium incorporation. Nitrogen sources inhibit the incorporation of calcium during the day, indicating that cellular ammonia production is probably not responsible for precipitation. The differential wash-out rates of calcium absorbed during the day compared to those at night support the concept of a 2-step mechanism for calcification.     

HALIMEDA HUMMII SP. NOV., HALIMEDA CRYPTICA V. ACERIFOLIA VAR. NOV. (CAULERPALES,CHLOROPHYTA), AND ADDITIONAL RECORDS OF HALIMEDA SPECIES FROM: PUERTO RICO1

A new species, Halimeda hummii, and a new variety of Halimeda cryptica Colinvaux and Graham both originally collected from the edge of the continental shelf on the southwest coast of Puerto Rico are newly described. The new species is irregular in its segment morphology and is the smallest species of Halimeda presently known. Halimeda cryptica var. acerifolia from deep water possesses distinctive segments resembling maple leaves. Halimeda copiosa Goreau and Graham and typical H. cryptica are also collected in deep water and are newly recorded from Puerto Rico.     

Species diversity and distribution of the calcareous green macroalgae Halimeda in Taiwan,Spratly Island,and Dongsha Atoll,with the proposal of Halimeda taiwanensis sp. nov.

The calcified green algal genus Halimeda is one of the most ecologically important but morphologically diverse seaweeds in sub-tropical and tropical waters. Because of its high morphological plasticity, the identification of Halimeda species based on morphological characters is challenging without the assistance of molecular analysis. To date, the species diversity of Halimeda in Taiwan and its overseas territories has not been investigated with the assistance of DNA sequencing, and this taxonomic knowledge gap should be filled. The present study initiates a systematic examination of the species diversity and distribution of Halimeda in Taiwan, Spratly Island, and Dongsha Atoll in the South China Sea, using DNA sequence data (plastid tufA gene and rbcL) and morphological data. Our DNA analyses revealed the presence of 10 Halimeda species (Halimeda borneensis, Halimeda cylindracea, Halimeda discoidea, Halimeda distorta, Halimeda macroloba, Halimeda minima, Halimeda opuntia, Halimeda renschii, Halimeda taiwanensis sp. nov., and Halimeda velasquezii) in the waters around Taiwan, Spratly Island, and Dongsha Atoll. The majority of the species could be readily distinguished by their morphological and anatomical characters. The proposed new species, H. taiwanensis, was differentiated not only by our algorithmic species delimitation analyses (statistical parsimony network analysis and automated barcode gap discovery), but also by its morphological features. The proposed new species differs from two externally resembled species, H. cuneata and H. discoidea, in having an undulated segment margin, the complete fusion of medullary siphons at the node, the lack of segment stalk, and the presence of a large primary utricle. Here, we present the up-to-date taxonomic account, molecular diversity, and geographical distribution of Halimeda spp. in Taiwan and associated areas of the South China Sea. Environmental factors that might drive the occurrence and latitudinal distribution of the species are also discussed.     

Productivity and nutrient relationships in psammophytic versus epilithic forms of Bryopsidales (Chlorophyta): comparisons based on a short-term physiological assay

Members of the green algal order Bryopsidales (= Caulerpales) are important calcifying agents of tropical reefs and comprise two fundamentally different life-form groups: (1) epilithic species with limited attachment structures and (2) psammophytic forms that have extensive subterranean rhizoidal systems. Because the shallow-water habitats of the former have relatively low nitrogen (N) to phosphorus (P_i) ratios compared to the pore waters of the sedimentary carbonate-rich substrata in which the latter are anchored, we hypothesized that epilithic forms should tend to be relatively more limited by N, while psammophytic species should tend to show P_i limitation. In partial support of the hypothesis, light-saturated net photosynthesis (P_max) in the epilithic forms, Halimeda opuntia, H. lacrimosa and H. copiosa, tended to be enhanced by N, while P_i was inhibitory or had no effect. In contrast, the psammophytic forms, Udotea sp., U. conglutinata, H. monde, H. tuna and H. simulans, tended to be stimulated more by P_i, whereas N had little effect. The utility of a bioassay to assess macroalgal nutrient limitation, based on a physiological response (net P_max) to short-term nutrient pulses, is demonstrated.     

Phylogeny and taxonomy of Halimeda incrassata,including descriptions of H. kanaloana and H. heteromorpha spp. nov. (Bryopsidales,Chlorophyta)

The tropical green algal genus Halimeda is one of the best studied examples of pseudo-cryptic diversity within the algae. Previous molecular and morphometric studies revealed that within Halimeda section Rhipsalis, Halimeda incrassata included three pseudo-cryptic entities and that the morphological boundaries between H. incrassata and Halimeda melanesica were ill-defined. In this paper, the taxonomy of H. incrassata is revised: two pseudo-cryptic entities are described as new species, Halimeda kanaloana and Halimed heteromorpha, while H. incrassata is redefined to encompass a single, monophyletic entity. Similarities and differences between the three species and H. melanesica are discussed. Monophyly of H. heteromorpha, which was questioned in a former study, is reinvestigated using sets of 32 ITS1–ITS2 and 21 plastid rps3 sequences and various alignment and inference methods. The phylogenetic relationships within Halimeda section Rhipsalis are inferred from nuclear 18S–ITS1–5.8S–ITS2 and concatenated plastid sequences (tufA & rpl5–rps8–infA) and interpreted in a biogeographic context.     

Notes on marine algae from Hateruma island,Ryukyu

This paper deals with a small collection of marine algae which the author gathered at Hateruma island, one of the southernmost islands of the Ryukyu groups. Twelve species are reported; seven of which,Udotea glaucescens, Codium ovale, Halimeda micronesica, H. fragilis, Ectocarpus laurenciae, Centroceras apiculatum andCeramium sympodiale, are recorded here for the first time in Japan, one of which,Feldmannia formosana, is proposed as comb. nov., the other four,Chlorodesmis haterumana, Struvea haterumensis, Centroceras japonicum andLophocladia minima, are described here as new species.     

Molecular systematics,historical ecology,and phylogeography of Halimeda (Bryopsidales)

Halimeda (Bryopsidales), a genus of calcified, segmented green seaweeds, abounds in reefs and lagoons throughout the tropics. To investigate phylogenetic, phylogeographic, and historic ecological relationships of the genus, the nuclear rDNA including the SSU and both ITS regions were sequenced. A maximum likelihood tree revealed the following: (1) there were anatomical and morphological synapomorphies for five well-supported lineages; (2) the last common ancestor of one lineage invaded sandy substrata; those of two other lineages established in wave-affected habitats, whereas the cenancestor of the remaining two lineages occupied sheltered rocky slopes. Yet, several species adapted to new habitats subsequently, resulting in several cases of convergence; (3) all lineages separated into Atlantic and Indo-Pacific daughters, likely resulting from the rise of the Panamanian Isthmus. Each daughter pair gave rise to additional convergent species in similar habitats in different oceans; (4) Halimeda opuntia, the only monophyletic pantropical species detected so far, dispersed from the Indo-Pacific into the Atlantic well after the closure event; (5) minor SSU-sequence differences across species and phylogeographic patterns of vicariance indicated a relatively recent diversification of the extant diversity. Cretaceous and Early Tertiary fossil look-alikes of modern species must then have resulted from iterative convergence.     

The deep-water species of Halimeda Lamouroux (Halimedaceae,Chlorophyta) from San Salvador Island,Bahamas: species composition,distribution and depth records

Caribbean species of Halimeda from the steep slopes of San Salvador Island, Bahamas, were collected along vertical transects between 25 and 255 m, on the northeast, northwest, west, southwest and south sides of the island, using the Harbor Branch Oceanographic Institution's submersible Johnson Sea Link I. The characteristics delineating species (segment and utricle size) were assessed for selected species, and the depth and western Atlantic distributions of the species reviewed. Halimeda copiosa was found to show a variation of surface utricle diameter with depth, with the deeper plants having 15% larger diameter utricles than the shallower plants. Of the seven species, one variety and one form of Halimeda studied from our submersible dive sites, H. copiosa, H. cryptica and H. gracilis grew to the greatest depths, from 120 to 150-m depths. H. lacrimosa var. globosa was found growing to 91 m, and H. tuna f. platydisca and H. discoidea to a depth of 73 m. Those of lesser depth, to 61 m, were H. goreauii, H. tuna f. tuna and H. lacrimosa var. lacrimosa. These represent substantial increases in depth distribution of the nine taxa found.     

Diversity of Halimeda (Bryopsidales,Chlorophyta) in New Caledonia: a Combined Morphological and Molecular Study

Halimeda is a genus of calcified and segmented green macroalgae in the order Bryopsidales. In New Caledonia, the genus is abundant and represents an important part of the reef flora. Previous studies recorded 19 species that were identified using morphological criteria. The aim of this work was to reassess the diversity of the genus in New Caledonia using morpho‐anatomical examinations and molecular analyses of the plastid tufA and rbcL genes. Our results suggest the occurrence of 22 species. Three of these are reported for the first time from New Caledonia: Halimeda kanaloana, H. xishaensis, and an entity resembling H. stuposa. DNA analyses revealed that the species H. fragilis exhibits cryptic or pseudocryptic diversity in New Caledonia. We also show less conclusive evidence for cryptic species within H. taenicola     

Chemical defense and chemical variation in some tropical Pacific species of Halimeda (Halimedaceae; Chlorophyta)

Over a dozen species of the genus Halimeda have been chemically investigated and found to produce the diterpenoid metabolites halimedatrial (1) and halimedatetraacetate (2) in varying concentrations. These meabolites have been proposed to play a role in chemical defense against herbivores based on their chemical structures and their demonstrated biological activities in laboratory and aquarium assays. We examined and compared the feeding deterrent effects of these two compounds tovard herbivorous fishes in field experiments on Guam reefs. Halimedatrial is a more effective feeding deterrent than halimedatetraacetate. It is the major secondary metabolite in young Halimeda macroloba and in the newly produced segments of growing plants. The organic extracts from young plants and new segments were significantly more deterrent than extracts from mature plant tissue. Some populations of Halimeda growing in reef-slope habitats, where herbivory is intense, also have high concentrations of halimedatrial. We compared extracts between reef slope and reef flat collections of Halimeda opuntia on Guam and Pohnpei (= Ponape), and H. discoidea and H. macroloba on Guam. We found that halimedtrial was the major metabolite in reef-slope collections of H. opuntia from Pohnpei and Pago Bay, Guam, and that halimedatetraacetate was the major metabolite a non-reef slope populations. In the cases examined, chemical defenses were greatest in (1) plant parts and (2) populations that were at greatest risk to herbivores.     

High morpho‐anatomical variability in Halimeda macroloba (Bryopsidales,Chlorophyta) in Thai waters

Halimeda macroloba is a common widespread and morphologically variable species in the Indo‐Pacific Ocean. A series of morphometric data (16 morphological and 46 anatomical variables) and the chloroplast‐encoded tuf A gene were examined to explore the morphological and genetic variations within the species and to better determine species boundaries in H. macroloba in Thai waters. Moreover, the environmental conditions, which may affect morphological variations in H. macroloba, especially of Haplotype I were examined. Our results showed that H. macroloba has more morpho‐anatomical variability and broader species boundaries than previously thought in several characters: holdfast type, segment shape and size, node height with differences in pore size, the presence of two additional patterns of peripheral utricle as seen in surface view, and additional layers of utricles (up to seven layers). Additionally, two new variable characteristics have been reported for the first time, i.e. shape and margin of peripheral utricles. Water depth and light correlated with thallus morphology, larger thalli and segments with a greater number of utricle layers were associated with subtidal plants, while smaller thalli and segments were found in the intertidal or high light intensity areas. The high plasticity of this species may explain why in the Indo‐Pacific Ocean this species is common and dominant.     

Growth rate,ultrastructure and sediment contribution of Halimeda incrassata and Halimeda monile,Nonsuch and Falmouth Bays,Antigua, W.I.

Halimeda incrassata and Halimeda monile, the two dominant rhipsalian Halimeda, were evaluated behind a bank barrier reef, in a fringing reef lagoon and in an open lagoon. Growth was calculated in number of segments, weight of segments and turnover rate. More than 1800 plants were stained with Alizarin Red-S dye, yielding average number of segments/plant/day and g CaCO₃/m²/year for each of the above areas of 2.17/114, 1.43/65.7 and 1.6/56.9, respectively. Average weight CaCO₃/segment was 4 mg. SEM revealed ultrastructure of short and long unoriented aragonite crystals forming in new segments within 24 h and an effective holdfast system with filaments partially coated with carbonate fragments. Greatest growth occurred within thin to medium density grass beds. In Nonsuch Bay sediment production from these two species alone was 0.057 mm/year or 1 1/2 orders of magnitude less than estimates of the total production from all Halimeda species (1.01 mm/year) over the past 6745 years.     

Interaction of herbivory and seasonality on the dynamics of Caribbean macroalgae

Many Caribbean coral reefs are undergoing a phase shift from coral to macroalgal dominance. Understanding the processes driving changes in algal abundance and community structure requires clarification of the relative effects of top-down (e.g., herbivory) and bottom-up processes (e.g., light, temperature, and nutrients). To date, a number of studies have examined the relative effects of grazing versus nutrification but interactions between herbivory and natural, seasonal fluctuations in temperature and light have not been investigated. This study considered the dynamics of three Caribbean macroalgal species [Lobophora variegata (Lamouroux), Dictyota pulchella (H?rnig and Schnetter), and Halimeda opuntia (Linnaeus)] and algal turf. A field experiment was established to measure species-specific algal dynamics (changes in abundance) over 13?months in the presence and absence of herbivory. Both herbivory and seasonal changes were important processes controlling macroalgal and turf abundance. Water temperature and light had a key role on D. pulchella; this species?? abundance significantly increased in the summer, when water temperature and light were the highest, and decreased during winter. Surprisingly, herbivory did not seem to control D. pulchella directly. However, herbivory was the most important process controlling the abundance of L. variegata, H. opuntia, and turf. The abundance of both algal species was correlated with seasonal changes in the environment, but was depleted outside cages throughout the year. The abundance of H. opuntia was positively correlated with temperature and light, but there was no statistical interaction between drivers. The statistical interaction between temperature and light was significant for the abundance of L. variegata and turf, but algal abundance declined as both factors increased. Overall, macroalgal and turf cover were mainly controlled by herbivory, while community structure (which species contributed to the overall cover) was largely influenced by seasonal changes in temperature and light.     

Algal contact as a trigger for coral disease

Diseases are causing alarming declines in reef‐building coral species, the foundation blocks of coral reefs. The emergence of these diseases has occurred simultaneously with large increases in the abundance of benthic macroalgae. Here, we show that physical contact with the macroalga Halimeda opuntia can trigger a virulent disease known as white plague type II that has caused widespread mortality in most Caribbean coral species. Colonies of the dominant coral Montastraea faveolata exposed to algal transplants developed the disease whereas unexposed colonies did not. The bacterium Aurantimonas coralicida, causative agent of the disease, was present on H. opuntia sampled close to, and away from diseased corals, indicating that the alga serves as a reservoir for this pathogen. Our results suggest that the spread of macroalgae on coral reefs could account for the elevated incidence of coral diseases over past decades and that reduction of macroalgal abundance could help control coral epizootics.     

Phenotypic plasticity and morphological adaptation of Halimeda opuntia (Bryopsidales,Chlorophyta) to light intensity

Plasticity gives plants the ability to adapt their morphology and growth to various environments. Environmental factors can lead to changes in the growth forms of algae. Halimeda opuntia was used as a model organism to determine the effects of highly irradiated and shade conditions in the field and its responses to low light conditions in the laboratory, which are known to be some of the main factors driving its morphological plasticity. To investigate the morphological and anatomical characteristics of the species, a total of 61 characteristics and 54 samples from Thailand, Japan and Indonesia were examined. In addition, we also tested the response under different light conditions in the laboratory. A phylogenetic tree was constructed using the tufA marker to confirm the species identification. We found that the thallus forms, branching patterns and segment shapes and sizes responded to the different light conditions. A brittle thallus network was found under shade conditions with low light intensity, while a compact thallus form was found under highly irradiated conditions. The H. opuntia segment shape was reniform under highly irradiated conditions, but its segments were adapted to be deeply trilobed in the lower thallus and tripartite shape in the upper thallus under shade conditions. The segment size also adapted; the segments in shaded areas were longer than those in sunny areas, which might have helped them increase their thallus height to ensure exposure to the high light habitat. This morphological variation and plasticity expanded our understanding of the range of H. opuntia plasticity present in the field and could help explain why this species is common and successfully colonizes various habitats worldwide.     

Geonemy,ecology, reproductive biology and morphology of the tardigrade <Emphasis Type="Italic">Hypsibius zetlandicus</Emphasis> (Eutardigrada: Hypsibiidae) with erection of <Emphasis Type="Italic">Borealibius</Emphasis> gen. n.

The morphology, biology and geographic distribution of Hypsibius zetlandicus (Murray 1907) are considered. Scanning electron microscopy (SEM) and/or light microscopy (LM) analyses have been carried out on H. zetlandicus and the type species of Hypsibius: Hypsibius dujardini (Doyère 1840), with particular emphasis on the buccal–pharyngeal apparatuses. Some unusual characteristics of this apparatus in H. zetlandicus lead us to the erection of the new genus Borealibius, to which H. zetlandicus (Borealibius zetlandicus comb. n.) is transferred. In the light of new discoveries of this species from polar, sub-polar and alpine regions, and based on the available bibliographic references, we hypothesize a boreo–alpine distribution for this species. The presence of traits that are unusual and rare (in other tardigrade species) have been observed whilst analyzing the reproductive biology and ecology of B. zetlandicus (i.e., the presence of hermaphroditism, parental care and the colonization of very different substrates).     

Halimeda biomass,growth rates and sediment generation on reefs in the central great barrier reef province

The average biomass ofHalimeda per m² of solid substratum increased progressively on a series of reefs situated at increasing distances from the shore in the central Great Barrier Reef. There was none on a reef close inshore, increasing to nearly 500 g m^?2 total biomass (?90% calcium carbonate) on an oceanic atoll system in the Coral Sea. The biomass measured contained 13 species ofHalimeda but was dominated by only two species,H. copiosa andH. opuntia, except on the atoll whereH. minima was dominant. Three sand-dwelling species were also present but did not occur anywhere in substantial quantities. Growth rates of the dominant species were measured bv tagging individual branch tips. A mean value of 0.16 segments d^?1 was recorded but 41% of the branch tips did not grow any new segments whilst only 1% grew more than one per day. The number of branch tips per unit biomass was very constant and has been used in conjunction with growth rates and biomass to calculate productivity rates, and thence sedimentation, in the lagoon of one of the reefs. Biomass doubling time of 15 d and production of 6.9 g dry wt m^?2 d^?1 are considerably higher than previously reported values forHalimeda vegetation and there was little seasonal change detected over a whole year. Those values indicate annual accretion of 184.9 g m^?2 year^?1 ofHalimeda segment debris over the entire lagoon floor (5.9 km²) of Davies Reef, equivalent to 0.13 mm year^?1 due toHalimeda alone, or 1 m every 1,892 years when other contributions to that sediment are taken into account.