Antimicrobial activity of extracts of Caribbean gorgonian corals

Extracts of 39 species of Caribbean gorgonians were tested for antimicrobial activity against 15 strains of marine bacteria. The bacteria consisted of three opportunistic pathogens, Vibrio parahaemolyticus, Leucothrix mucor, and Aerococcus viridans, and 12 strains isolated from either healthy or decayed gorgonians. Overall, only 15% (79 out of 544) of the tests resulted in antibacterial activity with 33% (13 out of 39) of the gorgonians inhibiting only one bacterial strain and 23% (9 out of 39) showing no activity. The extracts of four Pseudopterogorgia species showed relatively high levels of activity, inhibiting 43 to 86% of the bacterial strains. The potency of the active Pseudopterogorgia species was variable, however, and three additional Pseudopterogorgia species were inactive against all bacterial strains. With the exception of one sensitive strain, Vibrio species were resistant to gorgonian metabolites. Our results indicate that organic extracts of most Caribbean gorgonians do not possess potent, broad-spectrum antibacterial activity inhibitory to the growth of opportunistic marine pathogens and bacteria associated with healthy and decayed gorgonian surfaces. These findings suggest that the inhibition of bacterial growth is not the primary ecological function of gorgonian secondary metabolites and that bacteria may not be important selective agents in the evolution of gorgonian secondary chemistry.     

Reproductive patterns of scleractinian corals in the northern Red Sea

The majority of published accounts on scleractinian coral reproduction are from the tropical Pacific and Caribbean, with very little information known about Red Sea species. This report examines variation in reproductive mode in 24 species of hermatypic corals (belonging to seven families) in the Gulf of Eilat, Red Sea. Eighteen species are hermaphroditic broadcasters, two are hermaphroditic brooders and three are gonochoric broadcasters. In the Pocilloporidae, the gonads project into the body cavity, while in the other six families the gonads reside inside the mesenteries. The number of gonads per polyp in broadcasting species follows family or genus lines. Fecundity (eggs per polyp) increases with polyp size. Brooding species usually exhibit one or two gonads per polyp and each gonad contains only one to three oocytes. Oocyte size varies widely and does not relate to mode of reproduction. The largest oocytes (diameter = 450 μm) occur in the brooding coral Alveopora daedalea and in broadcasting species of the genus Acropora (diameter = 420 μm). Gonad morphology and gonochorism versus hermaphroditism appear to be constrained phylogenetically at the family or genus level. Lastly, this report compares the data presented for Red Sea scleractinian species with the data available on scleractinian corals from other geographical regions. Received: 2 February 1993 / Accepted: 9 March 1998     

Possible effects of water pollution on the community structure of Red Sea corals

The community structure and species diversity of hermatypic corals was studied during 1969–1973, in two reef flats in the northern Gulf of Eilat, Red Sea: the reef flat of the nature reserve at Eilat, which is chronically polluted by oil and minerals, and a control reef, located 5 km further south, which is free from oil pollution. In 1969, the nature reserve and the control reef had similar coral community structure. In September, 1970, both reefs suffered approximately 90% mortality of corals, as a result of an unexpected and extremely low tide. In 1973 the control reef was “blooming” with a highly diverse coral community, while almost no signs of coral recolonization have been observed at the nature reserve, and it is significantly lower in diversity. It is suggested that phosphate eutrophication and chronic oil pollution are the major man-made disturbances that interfere with coral colonization of the reef flat at the nature reserve. Although no direct evidence is provided that oil damages hermatypic corals, the data strongly suggest that chronic oil spills prevent normal settlement and/or development of coral larvae. It is possible that chronic oil, pollution results in either one or a combination of the following: (1) damage to the reproductive system of corals; (2) decreased viability of coral larvae; (3) changes in some physical properties of the reef flat which interfere with normal settlement of coral larvae.     

Community structure and species diversity of hermatypic corals at Eilat,Red Sea

This study investigates the community structure of reefbulding corals in terms of species composition, zonation and diversity patterns, as well as possible factors affecting the observed distributions. The study was carried out by a series of line transects run underwater with SCUBA apparatus from the reef flat to a depth of 30 m. The reefs of Eilat are of the fringing type, with seleractinian corals as the most important hermatypic organisms. The different zones of the reef are analyzed on the basis of topographical characteristics of the reef, as well as from the numerical data on abundance and living coverage, using cluster analysis of all transects surveyed. The present knowledge concerning species diversity is reviewed and analyzed in the context of hermatypic coral data. Three different diversity indices (the species count, Simpson's index and Shannon and Weaver's index) were calculated for estimating the diversity obtained on different zones of the reef. It was found that there is a successive increase in diversity of hermatypic corals from shallow water to a depth of 30 m. Species diversity and living voverage of corals were significantly greater in steeper zones as compared to flatter zones of the reef. A possible explanation for this phenomenon is the accumulation of sediments in the flat zones. It is proposed that the severe and umpredictable nature of the reef flat may account for low abundance and living coverage of corals. It is also proposed that deep-water species which do not invade shallow water are species which have developed high specialization to their local environment. The idea that light intensity is a significant factor in calcium-carbonate deposition by scleractinian corals is supported by field measurements of individual colonies at different depths.This paper is part of a thesis submitted to the State University of New York at Stony Brook in partial fulfillment of the requirements for a Ph. D. degree.     

Three party symbiosis: acoelomorph worms,corals and unicellular algal symbionts in Eilat (Red Sea)

Epizoic worms were found to occur on certain coral colonies from reefs off the coast of Eilat (Red Sea). We identified 14 coral species infested by acoelomorph worms at a depth range of 2–50 m. The host corals were all zooxanthellate and included both massive and branching stony corals and a soft coral. Worms from all hosts were identified as belonging to the genus Waminoa and contained two distinct algal symbionts differing in size. The smaller one was identified as Symbiodinium sp. and the larger one is presumed to belong to the genus Amphidinium. Worm-infested colonies of the soft coral, Stereonephthya cundabiluensis, lacked a mucus layer and exhibited distinct cell microvilli, a phenotype not present in colonies lacking Waminoa sp. In most cases, both cnidarian and Acoelomorph hosts displayed high specificity for genetically distinctive Symbiodinium spp. These observations show that the epizoic worms do not acquire their symbionts from the “host” coral.     

Lipids of some Caribbean and Red Sea corals: total lipid,wax esters,triglycerides and fatty acids

The Caribbean reef-building corals Porites porites (Pallas) and Montastrea annularis (Ellis and Solander) and the Red Sea corals Pocillopora verrucosa (Ellis and Solander), Stylophora pistillata (Esper) and Goniastrea retiformis (Lamark) were analysed for total lipid, wax ester and triglyceride content, and fatty acid composition. M. annularis contained about 32% of dry weight as total lipid, whereas much lower values of between 11 and 17% were recorded for the other four species. It is concluded that there is greater variation in coral total lipid than hitherto thought. The total lipid contained a substantial proportion of wax ester (22 to 49%) and triglyceride (18 to 37%). The storage lipids (wax esters and triglycerides) accounted for between 6 and 20% of the dry weight and between 46 and 73% of the total lipid. Variation in lipid content between species could not be attributed to geographical location, but the low values for total lipid in Red Sea corals may in part be due to environmental factors as these samples were collected in winter. All corals analysed contained high levels of saturated fatty acids, the most abundant fatty acids being 16:0, 18:0 and 18:1n-9. Marked differences were observed in polyunsaturated fatty acid (PUFA) content between species, with comparatively low levels of 10 and 11% of fatty acids being recorded in M. annularis and G. retiformis, respectively. The values for the other species ranged between 21 and 37%. Fatty acid composition may vary according to the proportions of fatty acids obtained from diet, algal photosynthesis and synthesis by the animal tissues.     

Use of pulse amplitude modulated (PAM) fluorometry for in situ measurements of photosynthesis in two Red Sea faviid corals

Measurements of the photosynthetic activity of symbiotic zooxanthellae in corals under natural growth conditions has been limited until recently, and this is one of the first reports on utilising a newly developed underwater pulse amplitude modulated (PAM) fluorometer (the Diving-PAM, Walz Gmbh, Germany) for such studies in situ. Photosynthetic responses to irradiance (photosynthetic photon flux, PPF) of the two faviid corals Favia favus (Forskål) and Platygyra lamellina (Ehrenberg) were measured while snorkelling or SCUBA diving (in August 1997), and we report here the results in terms of effective quantum yields of photosystem II (Y?) and estimated rates of photosynthetic electron transport (ETR, calculated as Y?×?0.5?× PPF?×?FA, where FA is the estimated fraction of light absorbed by the photosymbiont-containing tissue). Both species showed a reduction in Y with increasing actinic irradiances produced by the instrument above 500?μmol photons m^?2 s^?1, and the corresponding ETR values yielded apparently typical photosynthesis versus irradiance (P-I?) curves, which saturated between 1500 and 2000?μmol photons m^?2 s^?1. It was found that 30?s irradiation at each PPF level was sufficient to give optimal ETR values and, therefore, each P-I curve could be obtained within a few minutes. In situ point measurements from various areas of colonies under ambient light showed average ETR values within the range expected from the P-I curves. In order to test the Diving-PAM in an eco-physiologically relevant experiment, photosynthetic ETR versus PPF was measured for three sections of a large P. lamellina, each section of which received different natural irradiance levels. The results clearly demonstrated adaptations to the ambient light field in that vertical and downward-facing portions of the colony showed gradually lower maximal ETRs, steeper initial slopes of the P-I curves and, accordingly, lower light saturation points than upward-facing areas receiving higher light levels. Based on these trials, some evaluations are given as to the applicability of the Diving-PAM for photosynthetic measurements when monitoring similar corals.     

Migration,habitat use,and competition among mobile corals (Scleractinia: Fungiidae) in the Gulf of Eilat,Red Sea

We examined the impact of seven species of mobile mushroom corals (Fungiidae) on the community structure of sheltered reef slopes in terms of their patterns of migration, habitat use and competition with other benthic organisms. On fringing reefs at Eilat, Red Sea, polyps detached at 1 to 6 cm length, and grew to 11–55 cm length. Attached mushroom corals were oriented vertically in reef cavities. Detached corals migrated downward on the reef slope and onto rubble or soft substratum at the reef base, at 29 to 71 cmyr^–1. Mobility decreased with corallum size and extent of undersurface ornamentation. In aquaria, small corals righted themselves and migrated up to 6 cm d^–1 by nocturnally inflating and pushing their tissues against the substratum. Autonomous coral behavior and storm-generated water motion appeared to account for most fungiid mobility at Eilat. Mushroom corals did not damage each other upon contact, even in multi-species aggregations, but unilaterally damaged non-fungiid scleractinian corals. Their dominance during contact interactions retards overgrowth by larger attached scleractinians, and mobility allows them to colonize soft substrata not accessible to most other reef corals.     

Antimicrobial activities of marine sponges from the Mediterranean Sea

Extracts from marine sponges collected along the French coast of Mediterranean in 1983 have been tested for antibacterial and antifungal activities. The distribution of antimicrobial activities against five classes of microorganisms (5 Gram-positive and 5 Gram-negative terrestrial bacteria, 10 marine bacteria, 15 human pathogenic fungi and 5 phytopathogenic fungi) among 28 species of marine demosponges is reported. Antibacterial activity against Gram-positive bacteria (77%) is much more frequent than against Gram-negative bacteria (53%). Activity against marine bacteria and yeast is less frequent (32%). Those sponges which contain a large quantily of symbiotic bacteria display a weak antifungal activity.     

Sponge-inhabiting barnacles on Red Sea coral reefs

In this study eight different species of barnacles were found within nine species of sponges from the Red Sea. This brings to 11 the number of sponge-symbiotic barnacles reported from the Red Sea, two of these are new Acasta species (not described herein) and one (A. tzetlini Kolbasov) is a new record for this sea. This number is much higher than that of symbiotic barnacles found within sponges from either the N. Atlantic (2) or the Mediterranean (4). Two possible explanations for this are the presence of numerous predators in coral reefs and scarcity of available substrate for settlement. These factors can lead to high incidence of symbiotic relationships. Of the nine sponge species, only one (Suberites cf. clavatus) had previously been known to contain barnacles. Even at the family level, this is the first record of symbiotic barnacles in two out of the seven sponge families (Latrunculiidae, Theonellidae). Our present findings strengthen the apparent rule that the wider the openings in a barnacle shell, the fewer the host taxa with which it will associate, usually from one or two closely related families, and the more frequent it will associate with elastic sponges. Most Neoacasta laevigata found on Carteriospongia foliascens were located on the same side as the sponge's ostia, i.e. facing the incoming water. This adaptation allows the barnacles to catch more suspended particles from the water, provides them with more oxygen and prevents their exposure to discharged sponge waste. The highest density of barnacles observed on one face of a “leaf ” (with ostia) was 0.389 barnacles cm⁻² (one barnacle per 2.57 cm²) and on average 0.181 ± 0.68, while the average on the other side was only 0.068 ± 0.52 barnacles cm⁻². As indicated by the Morisita index, these barnacles most frequently (58%, n = 12) had a clumped spatial distribution (while the rest were randomly distributed), as is to be expected from such sessile organisms with internal fertilization via copulation. The presence of N. laevigata induced the growth of secondary perpendicular projections of its host C. foliascens. Of the N. laevigata examined, 17% brooded 324 ± 41 embryos each, of 286 ± 17 μm total length; only 5.7% (n = 123) were found to be dead. Size distribution analysis of skeletal elements from dead barnacles showed them to be significantly larger than the skeletal elements of the population of live barnacles ( p < 0.05). Received: 26 June 1998 / Accepted: 1 December 1998     

Bioactivity as an Options Value of Sea Cucumbers in the Egyptian Red Sea

Abstract:  The utility of a species can be divided into its direct, indirect, and options values. In the marine environment, direct consumptive values predominate and often lead to overexploitation at the expense of significant options values derived through bioprospecting for natural products. We surveyed the waters of the Egyptian Red Sea coast (Gulf of Aqaba [north] and the Red Sea [south]) for species of sea cucumbers and analyzed extracts from species for a range of bioactivities with potential biomedical applications. All habitat types were surveyed within these regions. We found 22 species of sea cucumber of which two, Holothuria fuscogilva and Holothuria flavomaculata , were recorded in Egypt for the first time. Although none of the species identified were unique to the Gulf of Aqaba, 10 species were only found in the Red Sea sector. Bioassay results showed that although no species had antibacterial activity, most extracts exhibited activity against Candida and Leishmania but were most active against a LoVo mammalian carcinoma cell line. Our most significant finding was the intraspecific variation in bioactivity in individuals collected from different habitat types and sectors of the coast. This variation may reflect the effect of environment on secondary metabolite production or may indicate significant genetic diversity between populations within a species. Our results indicate a potentially significant options value to sea cucumbers through bioprospecting. Given the importance of economic development in countries such as Egypt and the perceived low conservation value of invertebrates such as sea cucumbers, the linking of these factors to conservation is vital for the maintenance and sustainable exploitation of these animals .     

Littoral fauna of the Red Sea: the population of non-scleractinian anthozoans of shallow waters of the Red Sea (Eilat)

Approximately 22 species of sea anemones and 20 species of alcyonarians were found on the reef fringing the shallow water at Eilat (Gulf of Aqaba) and other localities along the Red Sea coast of the Sinai Peninsula. Investigations showed that these 2 groups of non-scleractinian coelenterates from (on different substrates) well identified colonies, part of them inhabiting sandy bottoms, other groups growing on the reef surface. Observations lead to the conclusion that several of the sea anemones and alcyonarians can act, under certain conditions, as factors limiting the development of hermatypic corals. In some areas, several species of the 2 groups of animals are found together with their symbiotic partners, such as fishes and crustaceans.This research has been sponsored partly by a grant from the Smithsonian Institution, No. SFC-7-0074 to L. B. Slobodkin (N. Y.) and L. Fishelson (T.-A.).     

New denitrifying bacteria isolated from Red Sea sediments

Sediments of various newly discovered deeps in the Red Sea were analyzed for the occurrence of denitrifying bacteria. The samples were collected in 1972 during the Valdivia cruises. Among the 27 different samples investigated, 17 revealed both coccoid and rod-shaped bacteria when enriched in complex nutrient broth (with 10% NaCl). Denitrifiers were recorded abundantly in the sediments, their population decreasing from some 10⁶/g in the surface material to only a few in the subsediment. A total of 16 pure cultures of denitrifying bacteria were isolated from the Suakin-and Thetis-deeps and studied morphologically, physiologically and biochemically. Genetics (molar percentage of guanine plus cytosine, % GC) and numerical taxonomy were included to reveal relationships and improve taxonomic classification. Fifteen isolates were described as Gram-negative, aerobic and facultative anaerobic (with NO ₃ ^- as H⁺-acceptor), polarly flagellated rods (Pseudomonas spp.); one was an inmotile, Gram-positive, facultative anaerobic coccus. None of the 15 Pseudomonas-isolates could be identified with one of the denitrifying species so far described and recognized. The strains should be regarded as hitherto undescribed denitrifying marine bacteria.Supported by the Bundesministerium für Forschung und Technologie, Bonn, Germany (FRG).     

Observations on mesopelagic fish from the Red Sea

Mesopelagic fish were collected from a cruise with the R.V. “Dr. Fridtjof Nansen” to the northern Red Sea and the interior Gulf of Aden off the Republic of Djibouti in March 1981. Off the Republic of Djibouti five species of mesopelagic fishes were caught and in the Red Sea six species. Benthosema pterotum (Alcock) were dominant in both areas. In the Red Sea Maurolicus muelleri (Gmelin) were also abundant. The mesopelagic fish caught in the Red Sea showed a pattern of vertical migration similar to that observed in other areas, in spite of the special hydrographical regime. The number of gill rakers of B. pterotum caught in the Red Sea differed significantly from that of all other populations studied. The number of photophores of M. muelleri apparently do not differ much from other populations. B. pterotum from the Red Sea mature at a larger size than other populations, while M. muelleri mature at a smaller size. The relative fecundity of M. muelleri is higher in the Red Sea than in other regions studied, while no significant difference was observed in B. pterotum. Both species appear to be opportunistic feeders. Their feeding chronology in the Red Sea seems to be similar to those observed in other areas.     

Community structure and vertical distribution of cyclopoid copepods in the Red Sea

The species abundance, vertical distribution and diurnal vertical migration of cyclopoid copepods was analyzed in the central Red Sea in October–November 1980. Samples were taken to a depth of 450 m with a multiple opening — closing plankton net with 0.1-mm mesh-size. Selected important species were allocated to five different groups according to their depth distributions during daytime. The greatest number of species (9) was found in the lower epipelagic zone (40 to 100 m), below the strong seasonal thermocline. The lowest number of species (1) occurred in the upper part of the upper mesopelagic zone (100 to 250 m), which is characterized by a strong dissolved oxygen gradient. Five species had a bimodal vertical distribution, with dual peak abundances in the epipelagic and upper mesopelagic zones. Distinct differences in distribution patterns were noted between sexes and/or developmental stages. The vertical range of diurnally migrating species was small, usually less than 50 to 100 m. Characteristic diurnal changes in the vertical succession of dominant species occur within the epipelagic zone (0 to 100 m). Species-specific vertical distribution patterns are compared with published data from other areas. A conspicuous difference in the proportion of carcasses was noted between species: small species (<0.5 mm in length) had a much higher proportion of carcasses, usually between 20 and 40% of the total standing stock, than larger ones (<5%). The potential causes of this phenomenon, which may be due to (1) methodological bias, (2) a lower sinking velocity of small carcasses, or (3) a higher mortality rate of small species, are discussed.     

Contents of heavy metals in marine algae from Egyptian Red Sea coast

Seaweeds belonging to 14 different genera of Chlorophyta, Phaeophyta and Rhodophyta were analyzed to determine the levels of heavy metals in two areas of the Egyptian Red Sea coast. Among the trace metals analyzed, Mn and Zn showed the highest mass concentrations in the surface seawaters of the two studied areas. However, algae obtained from Suez area had the highest concentrations of the investigated heavy metals than those collected from Mars Alam area. Nevertheless, a high variability of the metal levels occurs among the studied algae and also between the investigated areas. Moreover, Zn was the most abundant metal in the seaweeds of the Suez area, while Pb was predominant in Mars Alam area in red and brown algae. L. farinosa had the highest average concentration factor of Zn in Suez (29161 fold), while it was 20091 fold in E. intestinalis at Mars Alam. The highest value of metal pollution index (MPI) was recoded in L. farinosa (22.0) at Suez. It represents 4.6 fold of that value recorded in L. farinosa at Mars Alam. Among green, brown and red algae in Suez, the highest values of MPI were recorded in Cladophora (mixed sub-species) and H. comuto (18.2 and 18.3), P. pavonia (16.2) and L. farinosa (22.1), respectively; while at Mars Alam, they were recorded in Cladophora (mixed sub-species) (6.6), P. pavonia (3.4) and L. farinosa (4.8), respectively.     

Nontransitive patterns of historecognition phenomena in the Red Sea hydrocoral Millepora dichotoma

Allogeneic assays were conducted in situ on the Red Sea hydrocoral Millepora dichotoma. Forty-five pairwise combinations among ten colonies and ten control isografts were set up in four replicates each (180 and 40 pairs, respectively) and followed for up to 8 mo in the Gulf of Eilat, Red Sea in 1992–1993. In 42 allogeneic combinations we recorded a reproducible and unilateral tissue and skeleton overgrowth which developed within the first 10 wk up to 20 mm. Following the development of these primary overgrowths, four types of secondary responses were observed among most incompatible combinations: reversals in overgrowth directionality, tissue necroses, stand-offs and abnormal growth patterns. Secondary responses within a given set of replicates of most allogeneic combinations were characterized by high variability in type and intensity of response. Based on the outcomes of primary overgrowths, a complex nontransitive hierarchy was constructed for the ten colonies. All isografts and three allogeneic combinations fused within 3 wk. Fusion pattern between the three allogeneic combinations was nontransitive: one M. dichotoma colony repeatedly fused with two other colonies (four assays each). However, these two colonies not only did not fuse with each other, but one of them repeatedly overgrew its confrére. In the third compatible combination, the most superior and the most inferior colonies in the network of hierarchies among the ten colonies, fused in all tested assays. These results are compared with allogeneic outcomes in other enidarians, where nontransitive fusion between allogenic colonies have never been recorded.     

Spawning and development of three coral-associated Lithophaga species in the Red Sea

Lithophaga date mussels from three species (L. lessepsiana, L. simplex and L. purpurea) were removed from their stony coral hosts in the Red sea at Eilat, Israel. Spawning, observed in the laboratory on several occasions during 1987–1988, appeared to be closely tied to lunar periods, occurring primarily during the last quarter and the new moon. Embryonic and larval development was typical of that described for other mytilids and, except for pigmentation differences, which could be discerned during embryogenesis, the developmental stages of the three species were indistinguishable. Development to the pediveliger stage took 3 to 4 wk in standard culture conditions, but raising the temperature to 27.5 °C increased the growth rate of larvae of L. lessepsiana by as much as three-fold, so that the pediveliger stage was attained in 16 d. Larvae resulting from spawning by L. simplex adults removed from the coral Astreopora myriophthalma grew significantly faster in culture than larvac from adults removed from the coral Goniastrea pectinata (comparison of slopes, p<0.05). The latter individuals showed a 6-d growth plateau at the early umbone stage. Metamorphically competent larvae were capable of delaying metamorphosis for up to 4mo, which would allow an extended period for dispersion and would increase the chance of finding a suitable substratum in the natural environment.     

Stokes drift through corals

Motivated by shallow ocean waves propagating over coral reefs, we investigate the drift velocities due to surface wave motion in an effectively inviscid fluid that overlies a saturated porous bed of finite depth. Previous work in this area either neglects the large-scale flow between layers (Phillips in Flow and reactions in permeable rocks, Cambridge University Press, Cambridge, 1991) or only considers the drift above the porous layer (Monismith in Ann Rev Fluid Mech 39:37–55, 2007). Overcoming these limitations, we propose a model where flow is described by a velocity potential above the porous layer and by Darcy’s law in the porous bed, with derived matching conditions at the interface between the two layers. Both a horizontal and a novel vertical drift effect arise from the damping of the porous bed, which requires the use of a complex wavenumber k. This is in contrast to the purely horizontal second-order drift first derived by Stokes (Trans Camb Philos Soc 8:441–455, 1847) when working with solely a pure fluid layer. Our work provides a physical model for coral reefs in shallow seas, where fluid drift both above and within the reef is vitally important for maintaining a healthy reef ecosystem (Koehl et al. In: Proceedings of the 8th International Coral Reef Symposium, vol 2, pp 1087–1092, 1997; Monismith in Ann Rev Fluid Mech 39:37–55, 2007). We compare our model with field measurements by Koehl and Hadfield (J Mar Syst 49:75–88, 2004) and also explain the vertical drift effects as documented by Koehl et al. (Mar Ecol Prog Ser 335:1–18, 2007), who measured the exchange between a coral reef layer and the (relatively shallow) sea above.