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.     

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     

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.     

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.     

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.     

Calcification in the Green Alga Halimeda: IV. THE ACTION OF METABOLIC INHIBITORS ON PHOTOSYNTHESIS AND CALCIFICATION

The effects of a number of metabolic inhibitors on calcificationand photosynthesis in Halimeda tuna, H. discoidea, and H. macrolobaare described. The inhibitors used are CCCP, DNP, DCMU, azide,cyanide, chloramphenicol, cycloheximide, and Diamox. The effectsof these inhibitors, although complex, are consistent with ourmodel of calcification in Halimeda. Inhibition of photosyntheticCO₂ uptake inhibits calcification as does stimulation of respiratoryCO₂ evolution (i.e. uncoupling). There is also indirect evidencefor the presence of a possible light stimulated H⁺ efflux whichinhibits calcification. The observed calcification rate is thereforethe result of a number of factors which affect the concentrationof CO^–and the pH in the intercellular space of the Halimedathallus. The results obtained with the carbonic anhydrase inhibitor Diamoxprovide further evidence for the effective separation of theintercellular space from the external medium by the appressedperipheral utricles.     

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.     

Invertebrate Community Associated with the Macroalga Halimeda kanaloana Meadow in Maui,Hawaii

An expansive meadow of the native macroalga Halimeda kanaloana has been found in west Maui, Hawaii. This study examined the invertebrate community associated with the H. kanaloana meadow. Analyses of samples collected by SCUBA divers found that the meadow supports a diverse and unique benthic community. The meadow provides a suitable habitat for a variety of epibenthic and epifaunal invertebrates in the otherwise homogeneous sandy habitat. Infaunal polychaete abundances, species richness and Shannon‐Wiener diversity index were also higher inside the meadow. Abundances of epibenthic organisms, and dissimilarities of the polychaete assemblage, inside and outside the meadow were greater at deeper stations. This might be due to an effect of the Halimeda density rather than depth, suggesting that the macroalgal density might play an important role in shaping the benthic community. (© 2008 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

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.     

Photosynthesis and calcification in the calcifying algae Halimeda discoidea studied with microsensors

With microsensors, we measured the steady‐state microprofiles of O₂, pH and Ca²⁺ on the topside of young segments of Halimeda discoidea, as well as the surface dynamics upon light–dark shifts. The effect of several inhibitors was studied. The steady‐state measurements showed that under high light intensity, calcium and protons were taken up, while O₂ was produced. In the dark, O₂ was consumed, the pH decreased to below seawater level and Ca²⁺ uptake was reduced to 50%. At low light intensity (12 mmol photons m^‐2 s^‐1), Ca²⁺ efflux was observed. Upon light–dark shifts, a complicated pattern of both the pH and calcium surface dynamics was observed. Illumination caused an initial pH decrease, followed by a gradual pH increase: this indicated that the surface pH of H. discoidea is determined by more than one light‐induced process. When photosynthesis was inhibited by dichlorophenyl dimethyl urea (DCMU), a strong acidification was observed upon illumination. The nature and physiological function of this putative pump is not known. The calcium dynamics followed all pH dynamics closely, both in the presence and absence of DCMU. The Ca‐channel blockers verapamil and nifedipine had no effect on the Ca²⁺ dynamics and steady‐state profiles. Thus, in H. discoidea, calcification is not regulated by the alga, but is a consequence of pH increase during photosynthesis. Acetazolamide had no effect on photosynthesis, whereas ethoxyzolamide inhibited photosynthesis at higher light intensities. Therefore, all carbonic anhydrase activity is intracellular. Carbonic anhydrase is required to alleviate the CO₂ limitation. Calcification cannot supply sufficient protons and CO₂ to sustain photosynthesis.     

A new model for the calcification of the green macro-alga Halimeda opuntia (Lamouroux)

Halimeda opuntia is a cosmopolitan marine calcifying green alga in shallow tropical marine environments. Besides Halimeda’s contribution to a diverse habitat, the alga is an important sediment producer. Fallen calcareous segments of Halimeda spp. are a major component of carbonate sediments in many tropical settings and play an important role in reef framework development and carbonate platform buildup. Consequently the calcification of H. opuntia accounts for large portions of the carbonate budget in tropical shallow marine ecosystems. Earlier studies investigating the calcification processes of Halimeda spp. have tended to focus on the microstructure or the physiology of the alga, thus overlooking the interaction of physiological and abiotic processes behind the formation of the skeleton. By analyzing microstructural skeletal features of Halimeda segments with the aid of scanning electron microscopy and relating their occurrence to known physiological processes, we have been able to identify the initiation of calcification within an organic matrix and demonstrate that biologically induced cementation is an important process in calcification. For the first time, we propose a model for the calcification of Halimeda spp. that considers both the alga’s physiology and the carbon chemistry of the seawater with respect to the development of different skeletal features. The presence of an organic matrix and earlier detected external carbonic anhydrase activity suggest that Halimeda spp. exhibit biotic precipitation of calcium carbonate, as many other species of marine organisms do. On the other hand, it is the formation of micro-anhedral carbonate through the alga’s metabolism that leads to a cementation of living segments. Precisely, this process allows H. opuntia to contribute substantial amounts of carbonate sediments to tropical shallow seas.     

Distributional patterns of mobile fauna associated with Halimeda on the Tiahura coral-reef complex (Moorea,French Polynesia)

This study deals with the mobile fauna living associated with the turfs of three Halimeda species [H. incrassata, H. opuntia (three forms) and H. macroloba] from the Tiahura Reef complex. Ten 0.05 m² test areas of each Halimeda form have been randomly sampled from each geomorphological reef unit in order to obtain the specific abundance and biomass of different faunistic groups and species living within Halimeda populations. Then the raw data have been classified using the correspondence factor analysis to highlight the relationships between faunistic groups, or species, and the different Halimeda forms studied. The distributional patterns of the faunal communities seems to be controlled by the morphological features of the host-alga. The complex arborescent structure of the rhyzophytic H. incrassata species shelters fauna three times higher in abundance than other Halimeda heads. This fauna is mostly composed of a highly rich community of microcrustaceans and a very diversified community of Syllidae polychaetes. H. macroloba living on the outer reef flat retains a lot of small Nereidae polychaetes and a rich microgastropod assemblage. Dense H. opuntia tussocks (type A) on the fringing-reef and isolated H. opuntia fronds of pendulous chains (type B) on the barrier reef as well as beds of scattered H. opuntia (type C) on the outer reef flat provide environment for larger animals, and according to their zone of life, they retain very different faunal associations. Some ophiuroids, and some fish, collected in H. opuntia A and C, are newly reported from the Society Islands, French Polynesia, and the Pacific province. One Brachyurid species is presumably undescribed.     

Studies on Halimeda

Large areas of the inter-reefal seabed in the Great Barrier Reef are carpeted with vegetation composed almost entirely of the green calcareous alga Halineda. These meadows occur principally in the northern sections between 11°30 and 15°35S at depths of 20 to 40 m, but there are also some in the central and southern sections, where they have been found at depths down to 96 m. The vegetation is dominated by the same sprawling Halimeda species that are common on coral reefs in this region. However, on reefs these species grow on solid substrata, not soft sediments like the Halimeda-rich gravels that underlie the meadows. A total of 12 Halimeda species, together with two Udotea and one Penicillus species, are characteristic components of the shallow meadows. Below 50 m depth, species composition is restricted to only two major components. One, H. copiosa, is also important shallower, but the other is an unusually large and heavily calcified form of H. fragilis, a species that is normally a minor, fragile component of the shallow meadows. The maximum biomass found in these meadows was 4637 gm² of calcareous algae, although the thean for vegetated areas was 525 gm². These meadows are confined to the nutrient-depleted waters of the outer continental shelf just inside the outer barrier reefs, and are usually associated with distinct shoaling of the seabed caused by accumulation of thick deposits of calcareous Halimeda segments. The meadows are probably supported by very localized upwelling of nutrients from the adjacent Coral Sea onto the shelf, where they enrich the otherwise nutrient-depleted waters.Contribution No.367 from the Australian Institute of Marine Science     

Reef to basin sediment transport using Halimeda as a sediment tracer,Grand Cayman Island,West Indies

Fragments of the calcareous green alga Halimeda form a large part of the sediment in the fringing reef system and adjacent deep marine environments of Grand Cayman Island, West Indies. Nine species combine to form three depth-related assemblages that are characteristic of the major reef-related environments (lagoonpatch reef, reef terraces, and deep reef). These modern plant assemblages form the basis of the use of Halimeda as a sediment tracer. Halimeda-based tracer studies of Holocene sediments indicate that only sediments containing deep reef species of Halimeda are presently being transported through the reef system by sediment creep and being deposited at the juncture of the upper and lower island slope. Sediments containing shallow reef Halimeda are retained within the reef and lithified by marine carbonate cements. Tracer studies of Pleistocene sediment indicate large amounts of reef-derived carbonate sand containing deep water Halimeda were produced during interglacial high stands of sea level. Much of this material was removed by turbidity currents moving out of the reef system to the island slope down submarine channels perpendicular to the reef trend. These channels may still be identified on bathymetric profiles, but are no longer receiving coarse reef debris and are veneered with a blanket of pelagic carbonate mud.     

Larger foraminifera and sedimentation around Fongafale Island,Funafuti Atoll,Tuvalu

Larger foraminifera are an important component of coastal sediments around Fongafale Island, Funafuti Atoll, Tuvalu, and at least 10 species are present. In the shallow lagoon, foraminifera (mainly Amphistegina lessonii, A. lobifera, Baculogypsina sphaerulata, Calcarina spengleri, Marginopora vertebralis, and Sorites marginalis) are the dominant component of sand and gravel, followed in decreasing order of abundance by calcareous red and green algae, coral, and molluscs. In deeper water, Halimeda replaces the foraminifera. Close inshore, abrasion removes Halimeda and may reduce the number of foraminiferal tests. There is some sediment movement in both onshore and offshore directions although offshore transport appears minor. On land, dissolution that preferentially removes aragonite may increase the proportion of foraminiferal tests to as much as 83% of the subsurface sediment. Sediments on the ocean side are dominated by coral and coralline red algal debris thrown up in 1972 by cyclone Bebe and later moved inshore and lagoonward.Communicated by P.K. Swart     

A comparison of nutrient- and light-limited photosynthesis in psammophytic versus epilithic forms of Halimeda (Caulerpales,Halimedaceae) from the Bahamas

The relative nutritional status, with respect to phosphorus (P _i ) vs. nitrogen (N) limitation, and light-limited photosynthesis (P _s ) was examined over a broad range of quantum fluxes (I) for four Halimeda species, Halimeda tuna (Ellis and Solander) Lamouroux, H. simulans Howe, H. lacrimosa Howe and H. copiosa Goreau and Graham, taken from clear, shallow, Bahamian waters. The results support the hypothesis that psammophytic forms (i.e., sand dwellers anchored by a bulbous rhizoidal system) differ in nutrient status from epilithic forms (i.e., attached to rock by inconspicuous rhizoids). Maximum photosynthetic rates (P _max) for the epilithic species H. lacrimos and H. copiosa decreased (P<0.05) following P _i enrichment, but increased (P<0.05) following N pulses. Conversely, following brief exposures to P _i , P _max in the sand-dwelling forms H. tuna and H. simulans was elevated (P<0.05). These findings suggest that shallow species of Halimeda are adapted to take advantage of episodic nutrient pulses, and that partitioning of limiting resources may occur between the various life forms. Shallow water Halimeda species appear well adapted to variable light regimes, including low light conditions. In all cases, light-saturated photosyntheses (I _k ) occurred at irradiances much lower than the ambient levels available on typical sunny days. Associated with low saturation irradiances were low light requirements for photosynthetic compensation (I _c ) and reasonably efficient use of low photon flux densities as indicated by relatively steep slopes () of the P _s vs. I curves. Of the four species, H. copiosa was the most shade adapted, with considerably higher values and considerably lower I _c , I _k and photoinhibition values.     

Halimeda: paleontological record and palaeoenvironmental significance

Udoteacean algae, identical or related to Halimeda, have been recorded in shallow-marine carbonate rocks since Upper Triassic. About 30 species have been described, most of which occur in Lower Cretaceous shelf carbonates. These species are conventionally attributed to four “genera” (Arabicodium Elliott, Boueina Toula, Halimeda Lamouroux, Leckhamptonella Elliott), but the validity of these taxa is a matter of discussion (generic or subgeneric position, or synonyma of Halimeda?) owing to wide discrepancies in the classification of fossil and recent species of halimediform algae. The paleoenvironmental setting of the Mesozoic and the Tertiary is comparable with that of recent Halimeda: lagoonal as well as reefal environments are already known from Upper Triassic occurrences. A reinvestigation of Boueina limestones described from Norian-Rhaetian lagoonal carbonates of Western Thailand indicates the important role of the alga (Boueina marondei n. sp.) in sediment accumulation from its very beginnings.

     

The dispersal of Halimeda in northern hemisphere mid-latitudes: Palaeobiogeographical insights

The bryopsidalean alga Halimeda gained an important role as carbonate producer in Cenozoic tropical coral reefs and became a significant constituent of the modern Mediterranean seaweed flora. There are, however, open questions at which time the thermophile alga appeared in the cooler Mediterranean Sea and why it is not detected in coral reefs of the modern Persian Gulf. To unravel the biogeography and ecology of Halimeda at its northern margin of distribution, we use fossil Halimeda records of the Central Paratethys/Medditerranean for comparison of the geological, (palaeo)ecological and evolutionary dispersal constraints of the alga in the Miocene and Holocene Persian Gulf. The revealed spatial and temporal distribution patterns of Halimeda in the regions of the Mediterranean and Arabian seas identify water temperature as the major ecological constraint and the extreme Plio-Pleistocene climate changes as the motor for the dispersal and evolution of Halimeda in higher latitudes. Generally, the distribution of tropical species in higher latitudes was related to warm climate intervals during the Neogene. Accordingly, the available (palaeo)biogeographic data implies that the warm-adapted ancestors of the present-day Mediterranean H. tuna population possibly entered the Mediterranean Sea during the mid-Pliocene global warmth and became isolated during subsequent cooling. It also implies that the warm Persian Gulf water is probably unsuitable for the cool-adapted H. discoidea population in the Gulf of Oman and that its tropical ancestors could have reached the Gulf of Oman only during a Pleistocene glacial phase when monsoon-induced upwelling of cold water in the Arabian Sea was reduced and the Persian Gulf fell dry. This example demonstrates the limitation of the actualistic palaeontological approach when using biota at the edges of their distribution range as palaeoclimate proxy.     

Trace and minor element ratios inHalimeda aragonite from the Great Barrier Reef

The calcareous green algaHalimeda can be a substantial contributor to aragonite sediment in reef ecosystems. In contrast to coral aragonite, little is known about the trace and minor element composition ofHalimeda aragonite, so it is difficult to test oceanographic hypotheses about factors controlling its past growth. We investigated adapting trace element cleaning protocols for modern and HoloceneHalimeda aragonite, modern and HoloceneHalimeda trace and minor element compositions, and the potential utility ofHalimeda aragonite for paleoceanographic investigations. We successfully adapted and applied sample treatment protocols developed for measuring trace elements in coral aragonite (generally less than 500 y old) toHalimeda aragonite (modern to approximately 5000 y old in this study). ModernHalimeda aragonite from John Brewer Reef in the Central GBR had mean Cd/Ca ratios of 5.19 ± 1.68 nmol/mol forHalimeda micronesica and 2.35 ± 0.38 nmol/mol for three closely related species important in bioherm accumulationHalimeda copiosa, Halimeda hederacea, andHalimeda opuntia. Mn/Ca ratios, with means from 89–239 nmol/mol for these four species, showed both intra-and inter-specific variability. Sr/Ca ratios (10.9 ± O.1 mmol/mol) and Mg/Ca ratios (1.35 ± 0.26 mmol/mol) were similar for all samples. HoloceneHalimeda aragonite samples from cores of two bioherms in the northern GBR seemed well preserved on the basis of mineralogy and Sr/Ca and Mg/Ca ratios similar to those in modernHalimeda aragonite. Cd/Ca ratios (overall mean 0.96 ± 0.15 nmol/mol) were lower than those measured in the modernHalimeda from the central GBR location. However, Mn/Ca ratios in both cores were substantially higher than in modernHalimeda aragonite. While it may be possible to extract paleoceanographic information fromHalimeda aragonite, substantial care is needed to evaluate and avoid the effects of post-depositional alteration.