Publications (14)48.2 Total impact
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Article: Quality or quantity: is nutrient transfer driven more by symbiont identity and productivity than by symbiont abundance?
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ABSTRACT: By forming symbiotic interactions with microbes, many animals and plants gain access to the products of novel metabolic pathways. We investigated the transfer of symbiont-derived carbon and nitrogen to the sponges Aplysina cauliformis, Aplysina fulva, Chondrilla caribensis, Neopetrosia subtriangularis and Xestospongia bocatorensis, all of which host abundant microbial populations, and Niphates erecta, which hosts a sparse symbiont community. We incubated sponges in light and dark bottles containing seawater spiked with (13)C- and (15)N-enriched inorganic compounds and then measured (13)C and (15)N enrichment in the microbial (nutrient assimilation) and sponge (nutrient transfer) fractions. Surprisingly, although most sponges hosting abundant microbial communities were more enriched in (13)C than N. erecta, only N. subtriangularis was more enriched in (15)N than N. erecta. Although photosymbiont abundance varied substantially across species, (13)C and (15)N enrichment was not significantly correlated with photosymbiont abundance. Enrichment was significantly correlated with the ratio of gross productivity to respiration (P:R), which varied across host species and symbiont phylotype. Because irradiance impacts P:R ratios, we also incubated A. cauliformis in (13)C-enriched seawater under different irradiances to determine whether symbiont carbon fixation and transfer are dependent on irradiance. Carbon fixation and transfer to the sponge host occurred in all treatments, but was greatest at higher irradiances and was significantly correlated with P:R ratios. Taken together, these results demonstrate that nutrient transfer from microbial symbionts to host sponges is influenced more by host-symbiont identities and P:R ratios than by symbiont abundance.The ISME Journal 02/2013; · 7.38 Impact Factor -
Article: Benthic cyanobacterial bloom impacts the reefs of South Florida (Broward County, USA)
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ABSTRACT: Benthic cyanobacteria of the genus Lyngbya can form prominent mats and blooms in tropical and subtropical coral reef and seagrass habitats worldwide. A Lyngbya bloom on the reef tract offshore of Broward County, Florida, was first noted in 2002, and although it is seasonally variable in its distribution and abundance, it has persisted and spread over the past 3years. In this study, the most abundant species of Lyngbya found in the blooms have been identified and compared to other species of Lyngbya by morphological and molecular methods. The most common species of Lyngbya is consistent with the properties of Lyngbya confervoides C. Agardh. The 16S ribosomal DNA sequence shares 88–92% identity with other known Lyngbya sequences, suggesting that this bloom consists primarily of a new, previously unsequenced species of Lyngbya. The second most common Lyngbya in the bloom is consistent with Lyngbya polychroa. This persistent bloom is a concern because it smothers octocorals and other invertebrates and negatively impacts these southeastern Florida reefs.Coral Reefs 05/2012; 24(4):693-697. · 3.88 Impact Factor -
Article: Trade-offs in defensive metabolite production but not ecological function in healthy and diseased sponges.
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ABSTRACT: Diseases of marine organisms, and sponges in particular, are increasingly reported worldwide. Prior research indicates that the survival of sponges on reefs is due largely to their production of biologically active secondary metabolites that provide protection from a diversity of stressors. Aplysina Red Band Syndrome (ARBS) is an emerging disease affecting Caribbean rope sponges (Aplysina spp.), but it is not known whether secondary metabolites play a role in disease susceptibility and resistance. To investigate whether differences in secondary metabolites may explain variability in susceptibility to ARBS in Aplysina cauliformis, we used high performance liquid chromatography (HPLC) to generate chemical profiles from healthy tissue in both healthy and diseased sponges, and quantified peak areas for 15 metabolites. Analyses of healthy and diseased sponges revealed qualitative and quantitative differences in their chemical profiles. Aplysamine-1 and fistularin-3 were produced in significantly higher concentrations by healthy sponges, whereas aerothionin and 11-oxoaerothionin were found only in diseased sponges. At natural concentrations, extracts from both healthy and diseased sponges deterred feeding by an omnivorous reef fish. Fistularin-3 deterred feeding at concentrations found in healthy sponges, but not at concentrations found in diseased sponges. Aerothionin deterred feeding at concentrations found in diseased sponges, and may at least partially replace the loss of fistularin-3 as a feeding deterrent compound following pathogenesis, suggesting a trade-off in the production of feeding deterrent compounds. Extracts from healthy and diseased sponges inhibited bacterial growth, and both aplysamine-1 and fistularin-3 displayed selective antibacterial activity. Despite differences in secondary metabolite production between healthy and diseased sponges, the stress associated with ARBS does not appear to compromise the ability of A. cauliformis to maintain defenses against some of its natural enemies.Journal of Chemical Ecology 04/2012; 38(5):451-62. · 2.66 Impact Factor -
Article: Sponge-microbe symbioses: recent advances and new directions.
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ABSTRACT: Sponges can host abundant and diverse communities of symbiotic microorganisms. In this chapter, we review recent work in the area of sponge-microbe symbioses, focusing on (1) the diversity of these associations, (2) host specificity, (3) modes of symbiont transmission, and (4) the positive and negative impacts of symbionts on their hosts. Over the past 4 years, numerous studies have catalogued the diversity of sponge-microbe symbioses, challenging previous hypotheses of a uniform, vertically transmitted microbial community and supporting a mixed model of symbiont community transmission. We emphasize the need for experimental manipulations of sponge-symbiont interactions coupled with advanced laboratory techniques to determine the identity of metabolically active microbial symbionts, to investigate the physiological processes underlying these interactions, and to elucidate whether symbionts act as mutualists, commensals, or parasites. The amazing diversity of these complex associations continues to offer critical insights into the evolution of symbiosis and the impacts of symbiotic microbes on nutrient cycling and other ecosystem functions.Advances in Marine Biology 01/2012; 62:57-111. · 2.04 Impact Factor -
Article: Phylogenetic diversity, host-specificity and community profiling of sponge-associated bacteria in the northern Gulf of Mexico.
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ABSTRACT: Marine sponges can associate with abundant and diverse consortia of microbial symbionts. However, associated bacteria remain unexamined for the majority of host sponges and few studies use phylogenetic metrics to quantify symbiont community diversity. DNA fingerprinting techniques, such as terminal restriction fragment length polymorphisms (T-RFLP), might provide rapid profiling of these communities, but have not been explicitly compared to traditional methods. We investigated the bacterial communities associated with the marine sponges Hymeniacidon heliophila and Haliclona tubifera, a sympatric tunicate, Didemnum sp., and ambient seawater from the northern Gulf of Mexico by combining replicated clone libraries with T-RFLP analyses of 16S rRNA gene sequences. Clone libraries revealed that bacterial communities associated with the two sponges exhibited lower species richness and lower species diversity than seawater and tunicate assemblages, with differences in species composition among all four source groups. T-RFLP profiles clustered microbial communities by source; individual T-RFs were matched to the majority (80.6%) of clone library sequences, indicating that T-RFLP analysis can be used to rapidly profile these communities. Phylogenetic metrics of community diversity indicated that the two sponge-associated bacterial communities include dominant and host-specific bacterial lineages that are distinct from bacteria recovered from seawater, tunicates, and unrelated sponge hosts. In addition, a large proportion of the symbionts associated with H. heliophila were shared with distant, conspecific host populations in the southwestern Atlantic (Brazil). The low diversity and species-specific nature of bacterial communities associated with H. heliophila and H. tubifera represent a distinctly different pattern from other, reportedly universal, sponge-associated bacterial communities. Our replicated sampling strategy, which included samples that reflect the ambient environment, allowed us to differentiate resident symbionts from potentially transient or prey bacteria. Pairing replicated clone library construction with rapid community profiling via T-RFLP analyses will greatly facilitate future studies of sponge-microbe symbioses.PLoS ONE 01/2011; 6(11):e26806. · 4.09 Impact Factor -
Article: Preliminary assessment of sponge biodiversity on Saba Bank, Netherlands Antilles.
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ABSTRACT: Saba Bank Atoll, Netherlands Antilles, is one of the three largest atolls on Earth and provides habitat for an extensive coral reef community. To improve our knowledge of this vast marine resource, a survey of biodiversity at Saba Bank included a multi-disciplinary team that sampled fishes, mollusks, crustaceans, macroalgae, and sponges. A single member of the dive team conducted surveys of sponge biodiversity during eight dives at six locations, at depths ranging from 15 to 30 m. This preliminary assessment documented the presence of 45 species pooled across multiple locations. Rarefaction analysis estimated that only 48 to 84% of species diversity was sampled by this limited effort, clearly indicating a need for additional surveys. An analysis of historical collections from Saba and Saba Bank revealed an additional 36 species, yielding a total of 81 sponge species recorded from this area. This observed species composition is similar to that found on widespread Caribbean reefs, indicating that the sponge fauna of Saba Bank is broadly representative of the Caribbean as a whole. A robust population of the giant barrel sponge, Xestospongia muta, appeared healthy with none of the signs of disease or bleaching reported from other Caribbean reefs; however, more recent reports of anchor chain damage to these sponges suggests that human activities can have dramatic impacts on these communities. Opportunities to protect this extremely large habitat should be pursued, as Saba Bank may serve as a significant reservoir of sponge species diversity.PLoS ONE 01/2010; 5(5):e9622. · 4.09 Impact Factor -
Article: Phylogenetic and chemical diversity of three chemotypes of bloom-forming lyngbya species (Cyanobacteria: Oscillatoriales) from reefs of southeastern Florida.
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ABSTRACT: The cyanobacterial genus Lyngbya includes free-living, benthic, filamentous cyanobacteria that form periodic nuisance blooms in lagoons, reefs, and estuaries. Lyngbya spp. are prolific producers of biologically active compounds that deter grazers and help blooms persist in the marine environment. Here, our investigations reveal the presence of three distinct Lyngbya species on nearshore reefs in Broward County, FL, sampled in 2006 and 2007. With a combination of morphological measurements, molecular biology techniques, and natural products chemistry, we associated these three Lyngbya species with three distinct Lyngbya chemotypes. One species, identified as Lyngbya cf. confervoides via morphological measurements and 16S rRNA gene sequencing, produces a diverse array of bioactive peptides and depsipeptides. Our results indicate that the other two Lyngbya species produce either microcolins A and B or curacin D and dragonamides C and D. Results from screening for the biosynthetic capacity for curacin production among the three Lyngbya chemotypes in this study correlated that capacity with the presence of curacin D. Our work on these bloom-forming Lyngbya species emphasizes the significant phylogenetic and chemical diversity of the marine cyanobacteria on southern Florida reefs and identifies some of the genetic components of those differences.Applied and environmental microbiology 04/2009; 75(9):2879-88. · 3.69 Impact Factor -
Article: Cryptic diversity of the symbiotic cyanobacterium Synechococcus spongiarum among sponge hosts.
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ABSTRACT: Cyanobacteria are common members of sponge-associated bacterial communities and are particularly abundant symbionts of coral reef sponges. The unicellular cyanobacterium Synechococcus spongiarum is the most prevalent photosynthetic symbiont in marine sponges and inhabits taxonomically diverse hosts from tropical and temperate reefs worldwide. Despite the global distribution of S. spongiarum, molecular analyses report low levels of genetic divergence among 16S ribosomal RNA (rRNA) gene sequences from diverse sponge hosts, resulting either from the widespread dispersal ability of these symbionts or the low phylogenetic resolution of a conserved molecular marker. Partial 16S rRNA and entire 16S-23S rRNA internal transcribed spacer (ITS) genes were sequenced from cyanobacteria inhabiting 32 sponges (representing 18 species, six families and four orders) from six geographical regions. ITS phylogenies revealed 12 distinct clades of S. spongiarum that displayed 9% mean sequence divergence among clades and less than 1% sequence divergence within clades. Symbiont clades ranged in specificity from generalists to specialists, with most (10 of 12) clades detected in one or several closely related hosts. Although multiple symbiont clades inhabited some host sponges, symbiont communities appear to be structured by both geography and host phylogeny. In contrast, 16S rRNA sequences were highly conserved, exhibiting less than 1% sequence divergence among symbiont clades. ITS gene sequences displayed much higher variability than 16S rRNA sequences, highlighting the utility of ITS sequences in determining the genetic diversity and host specificity of S. spongiarum populations among reef sponges. The genetic diversity of S. spongiarum revealed by ITS sequences may be correlated with different physiological capabilities and environmental preferences that may generate variable host-symbiont interactions.Molecular Ecology 07/2008; 17(12):2937-47. · 5.52 Impact Factor -
Article: Phototrophic nutrition and symbiont diversity of two Caribbean sponge–cyanobacteria symbioses
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ABSTRACT: Coral reef sponges frequently harbor symbiotic cyanobacteria that can potentially benefit their hosts by providing supplemental nutrition. Although nutritional mutualisms have been documented for Indo-Pacific sponges, previous investigations suggest that Caribbean sponges obtain no nutritional benefits from their symbionts. We conducted field-based shading experiments to determine the effects of reduced irradiance on symbiont abundance and host growth in the Caribbean coral reef sponges Aplysina fulva and Neopetrosia subtriangularis, both of which host the unicellular cyanobacterium Synechococcus spongiarum. For both host species, 6 wk of shading significantly reduced chlorophyll a concentrations to less than half of those in control sponges. Shaded A. fulva individuals exhibited less than half the growth of control sponges. For N. subtriangularis, no significant differences in growth rates were observed between shaded and control sponges. Measurements of gross photosynthesis to respiration (P:R) ratios predicted that both host sponges were heterotrophic at low irradiances (<250 μmol m–2 s–1) and phototrophic at high irradiances (>500 μmol m–2 s–1), with measurements obtained at high irradiances likely to be more indicative of natural conditions. Phylo- genetic analyses of cyanobacterial internal transcribed spacer (ITS) ribosomal RNA gene sequences revealed 3 genetically distinct clades of S. spongiarum (designated A, B and C). Clade A symbionts were isolated exclusively from A. fulva, Clade B symbionts from both host sponge species and Clade C symbionts exclusively from N. subtriangularis. These findings demonstrate that Caribbean sponges associate with diverse clades of cyanobacterial symbionts that may confer variable nutritional bene- fits; in some cases, these symbionts appear to substantially enhance host growth rates.Marine Ecology Progress Series 01/2008; 362:139-147. · 2.71 Impact Factor -
Article: Phylogenetic analyses of marine sponges within the order Verongida: a comparison of morphological and molecular data
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ABSTRACT: Because the taxonomy of marine sponges is based primarily on morphological characters that can display a high degree of phenotypic plasticity, current classifications may not always reflect evolutionary relationships. To assess phylogenetic relationships among sponges in the order Verongida, we examined 11 verongid species, representing six genera and four families. We compared the utility of morphological and molecular data in verongid sponge systematics by comparing a phylogeny constructed from a morphological character matrix with a phylogeny based on nuclear ribosomal DNA sequences. The morphological phylogeny was not well resolved below the ordinal level, likely hindered by the paucity of characters available for analysis, and the potential plasticity of these characters. The molecular phylogeny was well resolved and robust from the ordinal to the species level. We also examined the morphology of spongin fibers to assess their reliability in verongid sponge taxonomy. Fiber diameter and pith content were highly variable within and among species. Despite this variability, spongin fiber comparisons were useful at lower taxonomic levels (i.e., among congeneric species); however, these characters are potentially homoplasic at higher taxonomic levels (i.e., between families). Our molecular data provide good support for the current classification of verongid sponges, but suggest a re-examination and potential reclassification of the genera Aiolochroia and Pseudoceratina. The placements of these genera highlight two current issues in morphology-based sponge taxonomy: intermediate character states and undetermined character polarity.Invertebrate Biology 09/2007; 126(3):220 - 234. · 1.31 Impact Factor -
Article: Impacts of Shading on Sponge-Cyanobacteria Symbioses: A Comparison between Host-Specific and Generalist Associations.
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ABSTRACT: The marine sponge Lamellodysidea chlorea contains large populations of the host-specific, filamentous cyanobacterium Oscillatoria spongeliae. Other marine sponges, including Xestospongia exigua, contain the generalist, unicellular cyanobacterium Synechococcus spongiarum. The impact of cyanobacterial photosynthesis on host sponges was manipulated by shading these sponge-cyanobacteria associations. If cyanobacteria benefit their hosts, shading should reduce this benefit. Chlorophyll a concentrations were measured as an index of cyanobacterial abundance. After two weeks, shaded L. chlorea lost more mass than controls, while shaded and control X. exigua did not lose a significant amount of mass. Chlorophyll a concentrations in shaded X. exigua were lower than in controls, but were not significantly different between shaded and control L. chlorea. In addition, L. chlorea shaded in situ lost over 40% of their initial area, but did not differ in chlorophyll a concentrations from controls. These results suggest that Oscillatoria symbionts benefit their host sponges in a mutualistic association. Synechococcus symbionts may be commensals that exploit the resources provided by their sponge hosts without significantly affecting sponge mass. When shaded, Synechococcus symbionts may be consumed by their hosts or may be able to disperse from this unfavorable environment. These data support the hypothesis that more specialized symbionts provide a greater benefit to their hosts, but hypotheses concerning the dispersal abilities of these symbionts remain to be explored. Sponge-cyanobacteria symbioses provide model systems for investigating the costs and benefits of symbiosis and the roles of dispersal, environmental conditions, and phylogenetic history in determining the specificity of endosymbionts for their hosts.Integrative and Comparative Biology 04/2005; 45(2):369-76. · 2.45 Impact Factor -
Article: Morphological, chemical, and genetic diversity of tropical marine cyanobacteria Lyngbya spp. and Symploca spp. (Oscillatoriales).
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ABSTRACT: Although diverse natural products have been isolated from the benthic, filamentous cyanobacterium Lyngbya majuscula, it is unclear whether this chemical variation can be used to establish taxonomic relationships among disparate collections. We compared morphological characteristics, secondary-metabolite compositions, and partial 16S ribosomal DNA (rDNA) sequences among several collections of L. majuscula Gomont, Lyngbya spp., and Symploca spp. from Guam and the Republic of Palau. The morphological characteristics examined were cell length, cell width, and the presence or absence of a calyptra. Secondary metabolites were analyzed by two-dimensional thin-layer chromatography. Each collection possessed a distinct cellular morphology that readily distinguished Lyngbya spp. from Symploca spp. Each collection yielded a unique chemotype, but common chemical characteristics were shared among four collections of L. majuscula. A phylogeny based on secondary-metabolite composition supported the reciprocal monophyly of Lyngbya and Symploca but yielded a basal polytomy for Lyngbya. Pairwise sequence divergence among species ranged from 10 to 14% across 605 bp of 16S rDNA, while collections of L. majuscula showed 0 to 1.3% divergence. Although the phylogeny of 16S rDNA sequences strongly supported the reciprocal monophyly of Lyngbya and Symploca as well as the monophyly of Lyngbya bouillonii and L. majuscula, genetic divergence was not correlated with chemical and morphological differences. These data suggest that 16S rDNA sequence analyses do not predict chemical variability among Lyngbya species. Other mechanisms, including higher rates of evolution for biosynthetic genes, horizontal gene transfer, and interactions between different genotypes and environmental conditions, may play important roles in generating qualitative and quantitative chemical variation within and among Lyngbya species.Applied and Environmental Microbiology 07/2004; 70(6):3305-12. · 3.83 Impact Factor -
Article: Biogeography of sponge chemical ecology: comparisons of tropical and temperate defenses.
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ABSTRACT: Examples from both marine and terrestrial systems have supported the hypothesis that predation is higher in tropical than in temperate habitats and that, as a consequence, tropical species have evolved more effective defenses to deter predators. Although this hypothesis was first proposed for marine sponges over 25 years ago, our study provides the first experimental test of latitudinal differences in the effectiveness of sponge chemical defenses. We collected 20 common sponge species belonging to 14 genera from tropical Guam and temperate Northeast Spanish coasts (Indo-Pacific and Mediterranean biogeographic areas) and conducted field-based feeding experiments with large and small fish predators in both geographic areas. We use the term global deterrence to describe the deterrent activity of a sponge extract against all of the predators used in our experiments and to test the hypothesis that sponges from Guam are chemically better defended than their Mediterranean counterparts. Sympatric and allopatric deterrence refer to the average deterrent activity of a sponge against sympatric or allopatric predators. All of the sponges investigated in this study showed deterrent properties against some predators. However, 35% of the sponge species were deterrent in at least one but not in all the experiments, supporting the idea that predators can respond to chemical defenses in a species-specific manner. Tropical and temperate sponges have comparable global, sympatric, and allopatric deterrence, suggesting not only that chemical defenses from tropical and temperate sponges are equally strong but also that they are equally effective against sympatric and allopatric predators. Rather than supporting geographic trends in the production of chemical defenses, our data suggest a recurrent selection for chemical defenses in sponges as a general life-history strategy.Oecologia 04/2003; 135(1):91-101. · 3.41 Impact Factor -
Article: Are benthic cyanobacteria indicators of nutrient enrichment? Relationships between cyanobacterial abundance and environmental factors on the reef flats of guam
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ABSTRACT: While benthic, filamentous cyanobacteria can be common on coral reefs, the factors influencing their distribution are poorly understood. Cyanobacterial blooms, like macroalgal blooms, may result from a combination of coastal eutrophication and reduced herbivory. Because benthic cyanobacteria are unpalatable to generalist herbivores, there may be little top-down control of cyanobacterial abundance. Since bottom-up factors may exert more influence on cyanobacterial populations, we hypothesized that high cyanobacterial abundance may be an indicator of high nutrient availability. In addition, cyanobacteria may compete with macroalgae for light and nutrients. Thus, we also hypothesized that cyanobacterial abundance may be negatively associated with macroalgal abundance. Since many strains of cyanobacteria wash ashore during periods of high wave action, we hypothesized that cyanobacterial abundance is negatively associated with wave height. We monitored cyanobacterial abundance, macroalgal abundance, nitrogen availability, phosphorus availability, salinity, and water temperature at nine reef flat locations around Guam. Average wave height for eastern and western shores, rainfall, minutes of sunshine, and wind speed were also monitored. Stepwise regression was used to determine which variable or combination of variables best explained variation in cyanobacterial abundance. Although nutrient availability was not significantly associated with cyanobacterial abundance, a positive association with macroalgal abundance explained 11.5% of the observed variation in total cyanobacterial abundance. At one site, negative relationships with macroalgal abundance and wave height explained 79.4% of the observed variation in the abundance of the cyanobacterium Oscillatoria margaritifera. Variation in cyanobacterial abundance can be best explained by examining individual strains of cyanobacteria, rather than by treating all cyanobacteria as a single ecological unit. Physical disturbance can be a more important influence on cyanobacterial abundance and distribution than either nutrient availability or interactions with macroalgae.Bulletin of Marine Science -Miami- 08/2001; 69(2):497-508. · 1.15 Impact Factor
Top co-authors
Top Journals
Institutions
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2012
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University of Mississippi
- National Center for Natural Products Research
Oxford, MS, USA
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2004–2012
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University of Alabama at Birmingham
- Department of Biology
Birmingham, AL, USA
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2003
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Spanish National Research Council
Madrid, Madrid, Spain
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